Progress in Oceanography 9295 (2012) 146165

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Progress in Oceanography
journal homepage: www.elsevier.com/locate/pocean

The inuence of upwelling variation on the spatially-structured euphausiid

community off central-southern Chile in 20072008
Ramiro Riquelme-Bugueo a,d,e,, Sergio Nez b, Erika Jorquera e,1, Lesly Valenzuela b,
Rubn Escribano c,d,e, Samuel Hormazbal f
a

Graduate Program in Oceanography, Faculty of Natural and Oceanographic Sciences, University of Concepcion, P.O. Box 160-C, Concepcion, Chile
Instituto de Investigacin Pesquera (INPESCA), P.O. Box 350, Talcahuano, Chile
Department of Oceanography, University of Concepcion, P.O. Box 160-C, Concepcion, Chile
d
Center for Oceanographic Research in the Eastern South Pacic (COPAS), University of Concepcion, P.O. Box 160-C, Concepcion, Chile
e
Pelagic Laboratory and Mesozooplankton (PLAMZ), Department of Oceanography, University of Concepcion, Concepcion, Chile
f
Department of Geophysics (DGEO), University of Concepcion, P.O. Box 160-C, Concepcion, Chile
b
c

a r t i c l e

i n f o

Article history:
Available online 14 July 2011

a b s t r a c t
This study assesses the spatial and temporal patterns of the euphausiid community from the coastal
upwelling zone and oceanic areas of central-southern Chile, surveyed between August 2007 and November 2008. A total of 22 species were found, most of them already described for the region. The numerically
dominant species was Euphausia mucronata for the entire study area (>60%), which was found in more
oceanic waters (>90W), thereby expanding its longitudinal distribution range. The species showed distinct spatial distribution patterns, allowing its classication as a coastal, oceanic, southern and northern
species. The community descriptors species richness, total abundance, Pielou and Shannon index all
had patterns associated with the cross-shelf and alongshore axes. Over a temporal scale, species abundance and community descriptors showed strong seasonal patterns. Abundances decreased offshore
but diversity increased towards the oceanic area, revealing an inverse relationship between total abundance and the Shannon index. Diversity was positively related to sea surface temperature. Although the
most abundant species were concentrated within the coastal zone, euphausiid abundance and diversity
in the oceanic region were high. Our ndings suggest that the high productivity of the upwelling region
may sustain the euphausiid populations in the coastal transition zone and in the offshore region, and that
high abundance and diversity across the entire region may be maintained by a highly heterogeneous
environment promoted by upwelling, giving rise to an increased number of potential ecological niches.
2011 Elsevier Ltd. All rights reserved.

1. Introduction
Zooplankton plays a key role in the pelagic food web by channeling phytoplankton production and structuring the pelagic ecosystem. Given the pivotal nature of the role played by these
organisms as a food source for larval and juvenile sh, the dynamics and distribution of zooplankton populations have a crucial
inuence on recruitment to sh stocks.
In marine systems, variations in biomass along a gradient of
environmental conditions are commonly accompanied by shifts
in the diversity and richness of marine species (Angel, 1993). In
coastal upwelling regions, these cross-shelf environmental gradi Corresponding author at: Graduate Program in Oceanography, Faculty of
Natural and Oceanographic Sciences, University of Concepcion, P.O. Box 160-C,
Concepcion, Chile. Tel.: +56 41 2661175; fax: +56 41 2207254.
E-mail address: rriquelm@udec.cl (R. Riquelme-Bugueo).
1
Present address: Biology Department, Dalhousie University, 1355 Oxford Street,
Halifax, Canada B3H 4J1.
0079-6611/$ - see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.pocean.2011.07.003

ents may have important effects on species diversity and richness

parameters, as well as on the standing stock biomass (Peterson and
Miller, 1977; Escribano and Hidalgo, 2000; Morgan et al., 2003,
Gmez-Gutirrez et al., 2005, Keister et al., 2009). In these ecosystems, the crustacean order Euphausiacea (better known as krill)
is an important component of the zooplankton, playing a pivotal
role in the economy of the pelagic food web of both oceanic and
coastal waters (Brinton, 1962; Mauchline and Fischer, 1969;
Antezana, 1970; Mauchline, 1980) constituting a potential top
down control over primary producers (Antezana, 2010) and being
important for the ux of organic carbon via direct exportation to
the sediments and by channeling it to higher trophic levels
(Gonzlez et al., 2009).
Some euphausiid species form dense aggregations in eutrophic
upwelling regions around the world and play a signicant role in
the trophodynamics of these ecosystems, transferring energy (biomass) from lower to higher trophic levels such as sh, seabirds and
marine mammals (e.g. Pillar et al., 1992; Arancibia et al., 1995;
Cury et al., 2000; Neira et al., 2004; Neira and Arancibia, 2004;

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Prez et al., 2006); however, euphausiids have typically low species richness (Gibbons et al., 1999). Other euphausiid species usually present low-density populations, forming small aggregations
or perhaps not swarming at all, and they are generally well
adapted to oligotrophic conditions (Gmez-Gutirrez et al., 1999).
The Humboldt Current System (HCS) is one of the most productive regions of the world ocean and supports an important shery
in the upwelling zone off Peru and Chile (Alheit and Bernal, 1993;
Montecino and Lange, 2009). Subsystems within the HCS are
already recognized by several authors (see Thiel et al., 2007 for a
review). One of these subsystems is the upwelling zone in central-southern Chile (3042S). In this zone, coastal upwelling is
highly inuenced by the high-pressure anticyclonic center of the
Eastern South Pacic (ESP); south-westerly winds cause upwelling,

147

mainly from austral spring to summer (September to mid-March),

and northerly winds promote downwelling in winter (Strub et al.,
1998). Likewise, coastal upwelling is inuenced by the coastline
and bathymetry of the continental shelf (40 km from the coast),
which is interrupted in certain places by submarine canyons (e.g.
Figueroa and Moffat, 2000; Sobarzo et al., 2001). Primary production rates are highest in this coastal zone (e.g., from 4 to
>20 g C m2 d1, Daneri et al., 2000; Montero et al., 2007), promoting signicant increments in zooplankton biomass (Escribano et al.,
2007). Also, mesoscale features (e.g. eddies and laments)
are frequent in this region (Correa-Ramirez et al., 2007, 2012;
Letelier et al., 2009). Eddies in this region can have an area of
6.5  103 km2 and they are formed near the coastal zone mainly
in springsummer with mean seaward speeds of 1.7 km d1

Fig. 1. Upper panel: Study area in the Humboldt Current System, Central/South Chile. Total area was divided into three zones for comparative purposes as shown by vertical
lines. Red, green and blue contour-lines are isobaths; i.e. 2000, 1000 and 300 m, respectively. Bottom panel: Temporal variability in euphausiid sampling, from September
2007 to December 2008. Rectangles indicate spatial location, and sampling season is indicated in the lower part. Different net types used in this study are shown.

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R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

(Correa-Ramirez et al., 2007). Both cyclonic and anticyclonic eddies

are frequent, but usually anticyclonic eddies are more persistent
(65 days) and transport a greater volume of water (0.34 Sv)
(Correa-Ramirez et al., 2007), and therefore they may be a potential source for the generation of retention mechanics for zooplankters, such as euphausiids, thereby increasing biological
productivity (Hormazbal et al., 2004; Correa-Ramirez et al.,
2007; Morales et al., 2007, 2010).
In the HCS, the euphausiid community is composed of 42 species (ca. 50% of all species) along an extensive latitudinal range
(from 5 to 52S, including the fjord region) and within a region
that may vary between 280 and 900 km from the coast (Antezana,
1978). Brinton (1962) grouped these species according to their
afnity for water masses; i.e. equatorial, central, transitional,
subantartic, Antarctic and boundary faunas. The zoogeographic
division of euphausiid species in the HCS was found to be similar
to the littoral faunal zonation (Antezana, 1981). In terms of
diversity, Antezana (1976) reported a spatially heterogeneous
euphausiid community for the fjord region and austral Chile
(4456S), as well as the existence of many ecological subsystems in that region. This is the only information available on the
spatial distribution and diversity of euphausiid species, although
it is based on samples obtained during the 1970s. Exceptionally,
Linacre and Palma (2004) and Palma and Silva (2004) reported
the spatial distribution of the most frequent euphausiid species
found, respectively, on the continental shelf off Concepcion
(36.5S) and in the fjord and channel region of southern Chile,
based on samples obtained in the 1990s. Since these studies, no
relevant information on euphausiid communities has been
published for the HCS, in particular for Chiles central-southern
subsystem, which has led to limited knowledge. More recent information, based on several compiled data sets, shows that the spatial
distribution of euphausiid species presents a pronounced variation
in the HCS according to latitude and offshore distance, presumably
as a response to the effect of water masses and currents; moreover,
species diversity seems to decrease from north to south and from
west to east (Ayn et al., 2009).
The knowledge of temporal and spatial community structure
variability in marine species is a rst step towards understanding
the effects of local productivity and trophodynamic interactions
among species. These processes are of great interest because they
can be suitable indicators of the structure and functioning of an
ecosystem and its potential relationship with ongoing global climate change, which is known to have consequences for marine
biological diversity. In this work, we assessed the spatial distribution and community structure of euphausiid species in the HCS,
emphasizing on both the coastal and oceanic waters of the coastal
upwelling zone of central-southern Chile (3045S) based on recently obtained samples. Since coastal upwelling appears as the
key process governing biological productivity in this region
(Escribano and Schneider, 2007), it is likely that distribution and
structure of the planktonic community may strongly depend on
the spatial and temporal variation of such process. We therefore
explored the link between the euphausiid community and the
environmental variability in the region over an annual cycle. We
thus aimed at understanding the spatial and temporal patterns of
euphausiid diversity and how they may respond to environmental
variation at a mesoscale and regional level.

2. Materials and methods

2.1. Study area and sampling
The study area is located in the coastal upwelling zone off central-southern Chile from 30 to 45S (northsouth axis) and from

72.7 to 93.7W (eastwest axis), equivalent to a grid of

1665  1850 km (Fig. 1). To better illustrate and understand the
spatial variability in our data and for comparative purposes, we divided our study area into three zones: the Coastal Zone (CZ), from
the coastline to 75.5W; the Transition Zone (TZ), from 75.6 to
78W; and the Oceanic Zone (OZ), from 78.1 to 94W (see
Fig. 1). These zones were established under the assumption that
bathymetry inuences the patterns observed in currents (e.g.
Sobarzo et al., 2001; Sobarzo and Djurfeldt, 2004), and therefore,
that it is likely that the pelagic biological community may also vary
depending on these zones, particularly between the CZ and OZ.
Cruises were conducted from August 2007 to November 2008
onboard different shing vessels of opportunity and onboard two
research vessels: Kay-Kay II (University of Concepcion) and AGOR
Vidal Gormz (Chilean Navy). During each one of these cruises, zooplankton samples were collected.
A total of 623 zooplankton samples were obtained during the
study period; 22.6% were from the CZ, 12.8% from the TZ, and
64.5% from the OZ. On a temporal scale, the zooplankton samples
were obtained mainly in November (42.4%) and December 2007
(28.7%), but sampling was carried out during virtually all the
months of the study period.
Cruises for plankton data were done at average intervals of
7 days (11 d, SD) during the study period from coastal (inshore)
to oceanic waters (offshore); the water column depth varied from
60 to 200 m and from >500 to 4000 m, respectively. Depending
on the availability or logistics of each vessel, zooplankton was collected using three types of nets: WP2 net (0.25 m2 mouth area and
200 lm mesh size), Bongo net (60 cm mouth diameter and 300 lm
mesh size), and Tucker Trawl net (1 m2 mouth area and 200 lm
mesh size). We used the WP2 net 78.7% of the times, the Bongo
net 12% and the Tucker Trawl net 9.3%. Zooplankton nets were
towed obliquely and/or vertically (when necessary) from near the
sea oor to the sea surface at coastal stations (inshore), and from
200 or 500 m depth to the sea surface at oceanic stations (offshore)
at a speed of ca. 0.5 m s1. A General Oceanic owmeter was used
to estimate the amount of water ltered by the nets in order to
standardize the total abundance of organisms. We obtained integrated samples from the water column and preserved them in a
10% buffered formalinseawater solution. Sampling was done in
daylight (52.3% of the time) and at nighttime (47.7%). Differences

Table 1
List of euphausiids species found in the study area from April 2007 to November 2008
off central-southern Chile. Code names were assigned for later analyses.
Species name

Authority

Code

Euphausia diomedeae
Euphausia gibba
Euphausia gibboides
Euphausia mucronata
Euphausia mutica
Euphausia recurva
Euphausia similis
Euphausia spinifera
Nematobrachion exipes
Nematoscelis atlantica
Nematoscelis megalops
Stylocheiron abreviatum
Stylocheiron afne
Stylocheiron carinatum
Stylocheiron elongatum
Stylocheiron longicorne
Stylocheiron maximum
Stylocheiron suhmi
Thysanoessa gregaria
Thysanopoda astylata
Thysanopoda obtusifrons
Thysanopoda orientalis

Ortmann, 1894
Sars, 1883
Ortmann, 1893
Sars, 1883
Hansen, 1905
Hansen, 1905
Sars, 1883
Sars, 1883
(Ortmann, 1893)
Hansen, 1910
Sars, 1883
Sars, 1883
Hansen, 1910
Sars, 1883
Sars, 1883
Sars, 1883
Hansen, 1908
Sars, 1883
Sars, 1883
Brinton, 1975
Sars, 1883
Hansen, 1910

EDIO
EGIB
EGIBBO
EMUC
EMUT
EREC
ESIM
ESPI
NFLE
NATL
NMEG
SABR
SAFF
SCAR
SELO
SLON
SMAX
SSUH
TGRE
TAST
TOBT
TORI

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

in sampling gear and methods of sampling are illustrated in Fig. 1.

Because of potential biases due to variable sampling gears, methods and day/night conditions, some corrections were applied and
comparisons of sampling gears were also tested, although as stated
above most samples were obtained with the WP2 net.
2.2. Laboratory procedure and species identication
In the laboratory, zooplankton samples were diluted to 810
times the total volume and subsampled with a Folsom plankton
splitter. Euphausiids were separated out from each subsample
and identied to the species level and developmental stage (as
far as possible and only for some species, listed more below). The

149

identication of euphausiid species was based on Brinton et al.

(2000), in digital format (CD Room from Expert Taxonomic Information, ETI BioInformatics; but also partially available online at
http://species-identication.org), which is a very helpful taxonomic tool since it facilitates the search for euphausiid species
by means of the Map it function (see CD Room from ETI for this
application). This function connes the search to a geographical
area of specic coordinates. The Map it function revealed 28
euphausiid species potentially present in our study area. We then
constructed our own pictographic taxonomic key based on records
of spatial distribution made by Antezana (1978) and according to
guides and drawings provided by Baker et al. (1990), Antezana
et al. (1976) and Brinton et al. (2000). Additionally, descriptions

Fig. 2. Composed hydrographic and environmental characterization for the study area from September 2007 to December 2008 off central-southern Chile. Upper panel: sea
level anomaly (SLA, in cm); Middle panel: sea surface temperature (SST, in C); Bottom panel: surface chlorophyll-a (Chl-a, in mg m3). Arrows indicate geostrophic current
eld (cm s1) and wind magnitude eld (m s1), for the upper and middle panels, respectively. Triangulation with Linear Interpolation was used as a data gridding method in
Surfer v.9.

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Table 2
Basic statistics for oceanographic and environmental variables in the study area from
April 2007 to November 2008 off Central Chile. Data were compared among zones for
total study period. SLA, sea level anomaly; GU, zonal geostrophic current; GV,
meridional geostrophic current; WU, zonal wind; WV, meridional wind; SST, sea
surface temperature; Chl-a, chlorophyll-a; SD, standard deviation; SE, standard error;
n, observation numbers. Positive or negative values correspond to velocities (currents
and winds) in direction to northward, southward, eastward and westward, as
appropriate.
Mean

Min

Max

SD

SE

Coastal zone
SLA (cm)
GU (cm s1)
GV (cm s1)
WU (m s1)
WV (m s1)
SST (C)
Chl-a (mg m3)

0.48
0.25
0.63
1.11
3.64
14.05
1.35

10.01
15.84
10.11
4.65
8.70
8.22
0.04

7.05
14.31
16.36
6.46
13.03
18.22
8.66

2.96
5.70
5.27
1.82
5.24
1.96
1.28

0.29
0.56
0.52
0.33
0.94
0.20
0.14

103
103
103
31
31
96
81

Transition zone
SLA (cm)
GU (cm s1)
GV (cm s1)
WU (m s1)
WV (m s1)
SST (C)
Chl-a (mg m3)

0.96
0.40
0.48
1.48
4.31
14.42
0.51

9.52
17.92
14.83
2.09
16.97
6.28
0.13

10.50
13.50
13.13
6.01
11.63
18.71
2.64

4.35
6.67
6.01
2.06
5.91
2.71
0.48

0.46
0.70
0.63
0.25
0.71
0.29
0.06

90
90
90
69
69
88
67

Oceanic zone
SLA (cm)
GU (cm s1)
GV (cm s1)
WU (m s1)
WV (m s1)
SST (C)
Chl-a (mg m3)

1.80
0.22
0.08
4.31
0.30
16.22
0.14

8.35
17.91
18.15
3.63
11.53
6.91
0.04

15.82
12.54
13.31
13.58
9.35
19.05
1.54

3.17
5.65
4.74
3.86
4.71
1.84
0.10

0.16
0.28
0.23
0.26
0.32
0.09
0.01

416
416
416
216
215
410
351

of E. mucronata larval stages (Antezana and Melo, 2008), the most

important and frequently found euphausiid species in the HCS
(Antezana, 1978, 2010), were used to complement the above
sources. Thus, we were able to identify 22 euphausiid species in
adult and subadult (juvenile) stages. Table 1 shows euphausiids
species found. Eggs and larval stages (i.e. nauplius plus metanauplius, calyptopis and furcilia) were identied and grouped without
distinction of species. Additionally, the most frequent euphausiid
species in our samples, i.e. E. mucronata, E. gibboides, Nematoscelis

Table 3
Day vs. night comparison between abundances of euphausiids species caught in the
study area. Signicant differences are showed (MannWhite test, <0.0001; <0.01;

<0.05). SE, standard error.

Emuc
Egib
Egibbo
Erec
Esim
Emut
Nmeg
Ne
Tgre
Sabr
Saff
Scar
Selo
Slon
Smax
Ssuh
Espi
Natla
Tast
Tobt
Tori
Edio

Day (n = 325)

Night (n = 298)

Mean

SE

Mean

SE

0.029
0.000
0.001
0.001
0.001
0.000
0.002
0.002
0.004
0.009
0.001
0.006
0.000
0.002
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000

0.048
0.001
0.002
0.005
0.001
0.001
0.002
0.001
0.001
0.003
0.001
0.002
0.000
0.000
0.001
0.000
0.000
0.000
0.000
0.000
0.000
0.000

0.205
0.007
0.019
0.019
0.004
0.004
0.009
0.001
0.009
0.024
0.002
0.014
0.000
0.001
0.004
0.001
0.001
0.000
0.000
0.000
0.000
0.000

0.050
0.001
0.003
0.005
0.001
0.001
0.002
0.001
0.001
0.003
0.001
0.002
0.000
0.001
0.001
0.000
0.000
0.000
0.000
0.000
0.000
0.000

Z adjusted

Night/day ratio

4.20
7.44
7.76
5.30
1.95
1.81
2.93
2.51
3.05
4.02
0.85
1.54
0.94
0.93
4.03
1.81
2.97
0.66
1.04
1.81
0.96
1.04

7.2
43.8
16.9
16.8
5.5
7.7
4.3
0.7
2.5
2.7
1.5
2.2
14.5
0.6
17.6
0
0
2.4
0
0
0
0

megalops, Stylocheiron abreviatum, S. carinatum, and Thysanoessa

gregaria, total length (TL) was measured from the tip of the
rostrum to the end of the telson and grouped into 1 mm size
classes.
2.3. Day vs. night abundance analyses
The abundance of each euphausiid species was standardized to
individuals per m3 according to the volume of ltered seawater.
Though sampling was done with three different net types, and
therefore different mesh sizes (200 vs. 300 lm mesh), we assessed
the effect of the net type with ANOSIM in PRIMER v6, but no significant differences were found (ANOSIM, p > 0.05), and therefore
conclude that the net type is not a source of error or bias in the

Fig. 3. Spatial/temporal variability in the SST (upper panel) and surface chlorophyll-a (bottom panel) throughout the study period (September 2007December 2008) for the
entire study area. Triangulation with Linear Interpolation was used as a data gridding method in Surfer v.9.

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R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Table 4
Basic statistics by zone for euphausiids species (adults and subadults as numbers per 1000 m3) from April 2007 to November 2008 in the study area off Central/South Chile.
Species

CZ (n = 141)

Emuc
Sabrc
Egibboc
Erecb
Scarb
Nmeg
Tgrea
Egiba
Esim
Smax
Emut
Saff
Ne
Slon
Espi
Selo
Ssuh
Natla
Tobt
Tast
Edio
Tori
UI

TZ (n = 80)

OZ (n = 402)

Total

Mean

SE

Mean

SE

Mean

SE

Mean

SE

842.5
7.3
11.8
47.1
0.8
17.1
1.1
11.5
3.0
1.8
0.0
0.0
0.1
0.4
0.0
0.3
0.0
0.0
0.0
0.0
0.0
0.2
0.0

192.4
2.7
8.8
21.8
0.6
4.6
0.4
11.2
1.9
0.9
0.0
0.0
0.0
0.3
0.0
0.3
0.0
0.0
0.0
0.0
0.0
0.2
0.0

89.2
0.8
1.3
5.0
0.1
1.8
0.1
1.2
0.3
0.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0

79.3
44.9
1.9
0.5
3.7
20.8
9.3
0.7
2.5
1.3
0.0
4.2
1.4
2.9
0.1
0.4
0.0
0.4
0.0
0.0
0.0
0.0
0.0

23.9
12.9
1.1
0.4
2.2
5.9
3.5
0.3
2.4
1.3
0.0
3.1
1.0
2.0
0.1
0.4
0.0
0.4
0.0
0.0
0.0
0.0
0.0

45.6
25.8
1.1
0.3
2.1
12.0
5.3
0.4
1.4
0.8
0.0
2.4
0.8
1.6
0.0
0.3
0.0
0.3
0.0
0.0
0.0
0.0
0.0

7.8
25.1
25.2
12.4
20.4
4.4
11.8
6.1
5.0
5.3
6.0
2.1
1.9
1.3
0.6
0.3
0.4
0.3
0.3
0.1
0.1
0.0
0.0

2.8
4.0
10.1
3.6
3.3
2.1
2.2
1.7
1.9
2.1
1.9
0.5
1.0
0.3
0.2
0.2
0.3
0.2
0.2
0.1
0.1
0.0
0.0

5.6
18.2
18.3
9.0
14.8
3.2
8.6
4.4
3.7
3.8
4.3
1.5
1.4
0.9
0.4
0.2
0.3
0.2
0.2
0.1
0.1
0.0
0.7

205.9
23.6
19.2
18.7
13.8
9.4
9.0
6.6
4.2
4.0
3.8
1.9
1.4
1.3
0.4
0.3
0.3
0.2
0.2
0.1
0.1
0.0
0.0

45.7
3.1
6.8
5.5
2.2
1.9
1.5
2.8
1.3
1.4
1.2
0.5
0.7
0.3
0.1
0.1
0.2
0.1
0.1
0.1
0.1
0.0
0.0

63.3
7.3
5.9
5.8
4.3
2.9
2.8
2.0
1.3
1.2
1.2
0.6
0.4
0.4
0.1
0.1
0.1
0.1
0.1
0.0
0.0
0.0
0.2

Species in bold indicate Upwelling Group.

CZ, coastal zone; TZ, transitional zone; OZ, oceanic zone; n, sample number; SE, standard error; %, relative abundance; UI, unidentied species.
a
Transitional Group.
b
Offshore Group.
c
North Group

presence/absence of species. However, since the euphausiid distribution in the water column is strongly inuenced by daily vertical
migration cycles, i.e., day vs. night (e.g. Antezana, 2002), and these
organisms also have the potential capacity to avoid zooplankton
nets in daylight (Brinton, 1967; Shaw and Robinson, 1998), we assessed signicant differences between day and night sampling
using ANOSIM in PRIMER v6. In order to estimate species-specic
night:day ratios for abundance data a MannWhite test was performed. These ratios were used as correction factors in day samples
to recalculate total abundance.
2.4. Species composition and diversity analyses
Total abundance of euphausiids for each sample regardless species was rstly estimated for the study area (N). Thereafter, the
species composition and diversity in the euphausiid community
were assessed by means of the species richness (S), i.e., the number
of different species within a given area or sample, the Shannon
diversity index (H0 ) i.e., the probability of the species distribution
within a given area or sample, and Pielous evenness index (J0 )
i.e., a measure of equitability or how evenly the individuals are distributed among the different species. The H0 index was computed
as follows:

H0 

S
X

pi log2 pi

where pi is the proportion of individuals from a sample unit belonging to species i, S is the number of species, and the summation is
from i = 1 to S. The J0 index was computed dividing H0 by ln(S). All
diversity indices were calculated in PRIMER v6 for each sample.

was used as to obtain sea level anomaly (SLA), zonal (u; crosshore)
and meridional (v, alongshore) geostrophic surface currents (GU
and GV, respectively), zonal and meridional winds (WU and WV,
respectively), surface Chlorophyll-a (Chl-a) and sea surface
temperature (SST). SLA, GU and GV data were obtained on the
merged weekly product of altimetry measurements by the
TOPEX-Poseidon, Jason-1, ERS-1/2 and Envisat satellites (1=4  1=4
degree of spatial resolution) distributed by AVISO (http://www.
aviso.oceanobs.com). SLA and geostrophic currents components
(u and v) were determined in each station by Linear Interpolation
from the nearest weekly value to the sampling date.
WU and WV data are based on QuickScat L3 daily gridded ocean
wind vectors (1=4  1=4 degree of spatial resolution) obtained from
the Jet Propulsion Laboratory SeaWinds Project (http://podaac.
jlp.nasa.gov). The speed in each station was determined by Linear
Interpolation of the u and v components corresponding to
sampling day.
Satellite Chl-a is based on SeaWiFS, MODIS-Aqua and MERIS
(resolution of 4 km at nadir) from the merged daily product of
Chl-a measurements distributed by the GlobColour Project
(http://www.globcolour.info). SST data is based on the 4 km
AVHRR Pathnder Project daily measurements (http://www.nodc.
noaa.gov/SatelliteData/pathnder4km). SST and Chl-a values corresponding to each station were determined by Linear Interpolation averaged over 3 days, centered at the sampling day of each
station. In order to visualize the environmental information, we
constructed spatial and temporal maps with Surfer v.9 software
(Golden Software Inc.) using the Triangulation with the Linear
Interpolation method by representing a good t for our environmental data.

2.5. Environmental data

2.6. Multivariate spatialtemporal analyses

In order to associate euphausiid abundance/distribution and

diversity with environmental conditions, satellite information

Longitude vs. latitude and time vs. longitude maps of euphausiid species abundance, development stages (eggs, nauplii plus

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metanauplius, calyptopis and furcilia) and community predictors

(S, N, H0 and J0 ) were generated using Surfer v.9 in order to observe
spatial/temporal distribution patterns. For presentation, nontransformed abundance data (number m3) were used. No
interpolation over the spatial and temporal domain was made for
abundance data because euphausiids form swarms and therefore
there is high probability of severe patchiness. However, we used

the Triangulation with Linear Interpolation in Surfer v9 as the

gridding method for the community predictors (S, N, H0 and J0 )
revealing the spatial and temporal patterns of the community.
We used multivariate analyses to explore the patterns in the
euphausiid community structure and their association to environmental factors. We constructed a species  sample/date matrix
that originally had 22 species  623 samples, with values in the

Fig. 4. Spatial distribution of most frequent euphausiid species collected in the study area. Numbers in legends are non-transformed abundance (n m3).

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

matrix equal to the density (# m3) of each species in each sample.

We used a classical approach from Field et al. (1982) and Clarke
and Warwick (2001) using PRIMER v6 software (Clarke and Gorley,
pp
2006). Prior to analysis, the data were
x transformed to normalize the variance while preserving distances among low values
(Field et al. 1982). Samples without euphausiids and species with
<5% of occurrence in the whole samples (i.e. rare species) were
removed from the analyses because of low representation and to

153

prevent them from having a strong inuence on the results. The nal matrix consisted of 15 species  348 samples. The cluster analysis was used to identify natural groupings in samples based on
their abundance similarities; a BrayCurtis similarity measure
and group average (Un-weighted Pair Group Averaging, UPGMA)
linkage method were used (Clarke and Warwick, 2001). Similarly,
a separate cluster analysis was performed on normalized environmental variables (e.g. SST, Chl-a, winds) using the Euclidean dis-

Fig. 5. Spatial distribution of rare euphausiid species collected in the study area. Numbers in legends are non-transformed abundance (n m3).

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tance measure and group average linkage method. The SIMPROF

application in Primer software was used to statistically assess the
different clusters and the SIMPER application was used to identify
which euphausiid species were responsible in the natural
grouping.
A non-metric multidimensional scaling (NMDS) analysis was
made and plotted as scatter-plots for taxonomic data and the environmental data then overlaid as gradients. These gradients are represented as vectors whose direction indicates the increment of the
attribute or variable, and the length corresponds to the degree of
correlation; i.e. short arrows mean low correlations and weak relationships between environmental variables and the NMDS space.
This procedure permits the comparison between environmentally and taxonomic grouped stations, and is useful in revealing
the mechanisms of variability in euphausiid distribution. NMDS is
considered to be one of the most robust ordination methods for
dealing with zero-zero species density pairs (e.g. Kruskal and Wish,
1978; Field et al., 1982; Gray et al., 1988). The most common measure that is used to evaluate how well (or poorly) a particular

conguration reproduces the observed distance matrix is the

stress measure. Thus, the smaller the stress value, the better
the t of the reproduced distance matrix to the observed distance
matrix. A stress value <0.1 is considered a good t (Clarke and
Warwick, 2001).
3. Results
3.1. Environmental condition
The study period covered a complete annual cycle, from winter
spring 2007 through spring 2008, in a region characterized by
strong seasonality in most oceanographic variables (Strub et al.,
1998; Sobarzo et al., 2007). Fig. 2 shows the spatial variability illustrating the upwelling conditions during the cruises based on sea
surface satellite data. Sea level anomaly was negative over the
coastal zone and mesoscale eddies were evident in the coastal
transition zone and over the oceanic region, revealing high levels
of kinetic activity upon upwelling circulation (Fig. 2, upper panel).

Fig. 6. Spatial/temporal variability in abundance of the most frequent euphausiid species throughout the study period. Numbers in legends are non-transformed abundance
(n m3).

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Meantime, southwesterly winds prevailed over the coastal zone in

the central portion of the region promoting coastal upwelling, as
evidenced by the cold plume extending off Concepcion to the offshore zone (Fig. 2, middle panel). Phytoplankton was mostly aggregated in the nearshore zone and appeared to increase in the
southern zone (Fig. 2, bottom panel).
So as to illustrate the differences in oceanographic conditions
among the three study zones, summary statistics of oceanographic
variables for each zone are shown in Table 2. These mean values
were obtained from the whole database, i.e. averaged over the entire study period.
The SST and Chl-a maps (shown in Fig. 3) represent average values (latitudes averaged) for an annual period, but there is certainly
temporal variation within this period. This variation is reected in
the yearly cycle, which shows the intensication of coastal upwelling in spring 2007 and spring 2008, as well as an apparent upwelling pulse in July 2008 (winter) and strong oceanic warming in
MarchApril 2008 (Fig. 3, upper panel), while Chl-a indicated

155

peaks in phytoplankton during the springs of 2007 and 2008

(Fig. 3, bottom panel).
3.2. Species and developmental stages composition
In total, 22 species were identied from all 609 samples collected. All the species had been reported previously for the ESP
(Antezana, 1978; Brinton et al., 2000), although we did not nd
Nyctiphanes simplex, a species reported as abundant and widely
distributed along the Chilean coast (Brinton, 1962; Antezana,
1978; Linacre and Palma, 2004). A signicant difference was
found between the day vs. night abundance (ANOSIM, p < 0.01)
and the MannWhite test reveled species-specic signicant differences so night:day ratios were calculated, as are shown in Table 3. The genera containing most species were Euphausia (8
species) and Stylocheiron (7 species), and E. mucronata was the
most abundant in all the samples, 63%, outnumbering the other
species with a total relative abundance of ca. 90% in the CZ, 46%

Fig. 7. Spatial/temporal variability in abundance of rare euphausiid species throughout the study period. Numbers in legends are non-transformed abundances (n m3).

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in the TZ, and 6% in the OZ (Table 4). Euphausia mucronata were

found in oceanic zones >90W thus expanding its longitudinal
geographic distribution. Nematoscelis megalops was abundant in
the TZ (12%) and S. abreviatum was also abundant, in both the
TZ (26%) and the OZ (18%). In the OZ, E. gibboides was most
abundant (18.3%) but S. carinatum also displayed important
abundance with ca. 15% (Table 4). The overall abundances of
all species found, separated by zones, are shown in Table 4. In
this summary the numerical dominance of E. mucronata becomes
more evident for the CZ and the TZ. The OZ exhibited a higher
variability in species abundance (Table 4).
Developmental stages abundance in the euphausiid community
were represented by signicant high abundances for eggs and calyptopis stages, with an average of 3715 and 3324 ind. per 1000 m3
in the CZ, respectively. Meanwhile, nauplius plus metanauplius
(NM) reach 162 ind. per 1000 m3 on average. Eggs, calyptopis
and NM represented 80%, 78% and 61% of the total in the CZ,
respectively. On the other hand, furcilia stages were more homoge-

neously distributed throughout all zones with 442 (22%), 423 (12%)
and 461 ind. per 1000 m3 (65%) in the CZ, TZ and OZ, respectively.
3.3. Spatial distribution of species and development stages
The spatial distribution of most abundant species revealed
marked differences in the geographical distribution among species.
Signicant differences were found among CZ, TZ and OZ (ANOSIM,
p < 0.01). Some species were clearly associated with the coastal
upwelling zone, i.e., E. mucronata and N. megalops (see Fig. 4),
whereas several others seemed to be more related to oceanic
waters. Among the oceanic species, S. carinatum, E. gibboides, and
E. recurva appeared to be the most restricted to the offshore zone,
unlike S. abreviatum, which was widely distributed over the complete region (Fig. 4). There was also differential distribution over
the alongshore axis. For example, S. carinatum and S. abreviatum
were more concentrated in the northern zone of the study area,
whereas T. gregaria were aggregated in the southern area (Fig. 4).
Similar distributional patterns were exhibited by rare species,
although most of them were found in the oceanic zone (Fig. 5).
Temporally, there were also differential distributions among
species. Concentrations of the dominant E. mucronata exhibited
maxima in spring 2007 and late summer 2008, but did not appear
in the CZ in spring 2008; several other abundant species presented
just one peak in summer 2008 (Fig. 6). Even though N. megalops cooccurred with E. mucronata in the CZ, these two species appeared
separately over a temporal scale: N. megalops exhibited peaks at
different times during the annual cycle (Fig. 6). Some other less
abundant species, and in more oceanic zones, also reached maxima
at different times of the year, but no clear seasonal pattern was observed, but rather they exhibited a single annual peak (Fig. 7).
Early developmental stages of euphausiids were also important
components during the surveys, because of their presence in all
study zones, although euphausiid eggs were more concentrated
in the CZ with ca. 80%. Meantime, the spatial patterns of the total
number of young stages of euphausiids, regardless of species, were
also examined (Fig. 8). Most eggs, calyptopis and nauplii were
aggregated in the CZ, probably because they belong to the numerically dominant coastal species, although calyptopis were more
widely spread throughout the region (Fig. 8). On a temporal scale,
both eggs and nauplii co-occurred and showed maxima in the
spring of each year, revealing this to be the reproductive season
(Fig. 9). Metanauplii and calyptopis were found after the maximal
abundances of eggs and nauplii, somehow reecting the development of the cohorts (Fig. 9).
3.4. Community descriptors

Fig. 8. Spatial distribution of developmental stage (eggs, nauplius plus metanauplius, calyptopis and furcilia) of euphausiid species collected in the study area.
Numbers in legends are non-transformed abundance (n m3).

Species richness (S), the Shannon index (H0 ), total abundance

(N), and the Pielou index (J0 ) were all used as proxies to assess
the spatial and temporal patterns of the community structure. Signicant differences among the three dened zones were found
(ANOVA, F = 11.5; df = 436; p < 0.0001) in terms of S, N, J0 and H0 .
A Tukey HSD post hoc test for unequal samples sizes was applied.
The results from this test indicated that S was signicantly different (p = 0.046) between the CZ and OZ and that N, J0 and H0 were
highly and signicantly different (p 6 0.01) among the CZ, TZ and
OZ, but not between the latter two (p > 0.2). The TZ had less diversity and lower abundances, probably due to the number of observations/samples, whereas S was maximal in the offshore region
(Fig. 10a). When plotting these descriptors over the spatial scale,
the patterns were not very clear. For instance, N was clearly higher
in the CZ (Fig. 10b) and the Pielou index reected a cross-shelf increase (Fig. 10c), although that pattern was difcult to infer from S
and H0 (Fig. 10a and d, respectively).

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157

Fig. 9. Spatial/temporal variability of developmental stage of euphausiid species throughout the study period. Numbers in legends are non-transformed abundances (n m3).

The variability of the community descriptors over the temporal

scales appeared to be mostly coupled to seasonality. Species richness followed an inverse pattern from that of N (Fig. 11a and b,
respectively), whereas N followed the pattern observed in E.
mucronata, the most abundant species in the CZ (Fig. 11b). Interestingly, H0 and J0 followed the same pattern as S and were characterized by sudden increases in diversity at different times of year, but
mainly concentrated in the summer and spring periods (see
Fig. 11c and d).
Size structure was also an important community descriptor. In
this case, the size distribution of each population reected the
age structure over the study period and over the spatial scale. Euphausia mucronata, for example, showed similar size structures for
the OZ and TZ with the <5 mm size class being the most frequent,
but the CZ seemed to concentrate the larger-sized individuals
(>15 mm); perhaps the whole population was better represented
in this zone (Fig. 12). The others abundant species did not show
much variation in age (size) structure among zones, except for E.
gibboides, whose population was poorly represented in the TZ in
terms of age structure (Fig. 12). Nematoscelis megalops was another
euphausiid species relatively well represented in its size frequency
distribution, with the 1520 mm size class better represented in all
zones (Fig. 12).
In terms of species linkages, cluster analysis allowed the grouping of nine statistically distinct hierarchical assemblages (SIMPROF, p < 0.01; Fig. 13). From SIMPER application we obtained
the species names in each cluster and their percentage contribution: Cluster a, T. gregaria (97%); Cluster b, T. gregaria (55%)
and E. gibba 33%); Cluster c, N. megalops (98%); Cluster d, E.
mucronata (84%); Cluster e, S. carinatum (99%); Cluster f, E.
recurva (87%); Cluster g, S. abreviatum (46%) and T. gregaria
(43%); Cluster h, S. abreviatum (94%); and Cluster i; E. gibboides

(51%), S. abreviatum (23%) and S. carinatum (13%). From the similarities in these clusters we constructed four groups according to their
spatial distributions: Coastal Transitional Group (T. gregaria, E. gibba), Coastal Upwelling Group (E. mucronata, N. megalops), Offshore
Group (S. carinatum, E. recurva) and North Group (E. gibboides, S.
abreviatum). The remainder species did not contribute signicantly
to any grouping or overlap in more than one group.
3.5. Environmental inuences
A NMDS analysis was applied to the whole species assemblage
along with environmental variables. Fig. 14 shows the plots of
three derived dimensions from the NMDS analysis. A stress value
of 0.08, from this analysis, can be considered as signicant and a
good t (Clarke and Warwick, 2001). This analysis made possible
the visualization of the associations among environmental factors
and euphausiid species diversity. In this way, we determined a
strong relationship between some species groups, such as E.
mucronata and N. megalops, and Chl-a and alongshore wind, i.e.
upwelling-favorable winds (see groups c and d in Fig. 14), in
contrast with other species groups a, e and f represented
by T. gregaria, S. carinatum, E. recurva and E. gibboides, which seem
to be more positively associated with SST, and therefore with offshore distance (Fig. 14). The rest of the species did not seem to
be associated with these variables (Fig. 14). In any case, offshore
distance should relate to some of the community descriptors because of the observed cross-shelf patterns (see Fig. 10). The relationship between distance to shore, the associated variables
temperature and Chl-a, and some of the community parameters
is shown in Fig. 15. Both J0 and H0 increased signicantly with offshore distance (Fig. 15d and e, respectively), whereas egg abundance (representing reproductive activity) showed an increasing

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showed a strong relationship with oceanic waters and upwelling-favorable winds (Table 5). Community descriptors were also
signicantly correlated to SST, conrming the increase in diversity, i.e. the H0 index, and decrease in abundance towards the offshore region (Table 5). On the other hand, S was signicantly
associated with an increase in latitude (Poleward) but the H0 index showed an opposite relationship (Equatorward). All these
signicant correlations evidenced the inuence of oceanographic
variability in structuring the euphausiid community over the
entire study area.

4. Discussion

Fig. 10. Spatial distribution of (a) total species (S), (b) non-transformed total
abundance (N, in n m3), (c) Pielou index (J0 ) and (d) Shannon index (H0 ) for the
euphausiid community present in the study area. Triangulation with Linear
Interpolation was used as a data gridding method in Surfer v.9 for S, J0 and H0 .

trend shoreward (Fig. 15c). On the other hand, J0 was positively related to SST (Fig. 15b), indicating that more species were found in
warmer waters and suggesting temperature-dependent spatial
heterogeneity, whereas eggs were weakly but signicantly correlated to surface Chl-a (Fig. 15a).
In order to examine in more detail the inuence of oceanographic variables on species abundances and community
descriptors, a stepwise multiple regression analysis was applied
on log-transformed abundances and oceanographic variables. All
oceanographic variables dened above were signicantly correlated to euphausiid abundance, although latitudinal and longitudinal gradients, zonal and meridional winds, SST and Chl-a
seemed to explain most of the variance (Table 5). For example,
E. mucronata showed a signicant and negative relationship with
SST (cold waters) implying it might be an upwelling species, but
showed a stronger association with distance from coast and
Chl-a, demonstrating it to be a predominantly neritic species
and associated with food-rich centers (Table 5). In turn, furcilia

When analyzing the spatial and temporal distribution patterns

of euphausiids, it is important to account for the sampling methods
and gear as sources of variability. Euphausiids are known to be
capable of avoiding being caught in zooplankton nets, especially
during daytime sampling (Brinton, 1967), and many species can
perform extensive vertical migrations during the day-night cycle
(DVM) (e.g. Antezana, 2002, 2009). Our study included daytime
and nighttime samples, and the daytime samples may have been
affected by both net avoidance and DVM beyond the sampled stratum (usually the upper 200 m). Diel effects on abundance estimates were indeed substantial and highly signicant, justifying
the need to apply correction factors to daylight samples, as suggested in other studies (Shaw and Robinson, 1998; Mackas et al.,
2004; Ware and Thomson, 2005). The use of different sampling
gear may also have affected our abundance estimates. For example,
the WP2 net was perhaps the most likely to be avoided by the target species. To reduce this potential error, we used this net for oblique tows and at speeds >0.5 m s1. Bongo nets, on the other hand,
are more commonly used to capture euphausiids (e.g. GmezGutirrez et al., 1999, 2005; Antezana, 2009) because such nets
can be towed at higher speeds (>0.8 m s1). However, the Tucker
Trawl net seems to be most efcient for capturing large-sized
zooplankton (see Shaw and Robinson, 1998) because of the greater
mouth opening (1 m2) and towing speed (ca. 1 m s1), which
allows larger volumes (>300 m3) of water to be ltered by each
net during the approximately 20-min tows (Escribano et al.,
2007). We should also note that the use of 300 lm mesh size
allows the capture of all developmental stages of euphausiids
and the probability of missing some eggs or nauplii of smaller species is rather low. In effect, most eggs and nauplii of E. mucronata
are greater than 600 lm in diameter (unpublished data).
All the species found in this study have been previously described for this region (Antezana, 1978; Brinton et al., 2000), however for the rst time E. mucronata was found inhabiting more
oceanic waters (>90W), thereby expanding their longitudinal distribution, although our results conrm that this species is essentially neritic (see Table 4) associated with high-food and
upwelling centers (see Figs. 2, 4 and 14). The absence of Nictyphanes simplex, however, deserves some consideration. This species
was previously reported to be highly abundant in Chiles coastal
zone (Antezana, 1978; Linacre and Palma, 2004) but a recent study
in the HCS based on samples obtained in 2000 (Mujica and Pavez,
2008) did not report the presence of N. simplex, although it could be
presumably present in northern Chile (A. Mujica, UCN, personal
communication). Our large euphausiid survey covered both coastal
and oceanic areas of central-southern Chile over an entire annual
cycle. The identication of this species was also straightforward,
it is unlikely to be confused with other similar species in the study
area (Baker et al., 1990; Brinton et al., 2000). In this context, it may
be necessary to review the present distribution of the euphausiid
community in the HCS. In fact, the geographical distributions that
are usually cited are based on surveys performed 30 years ago or

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

159

Fig. 11. Spatial/temporal variability of (a) total species (S), (b) non-transformed total abundance (N, in n m3), (c) Pielou index (J0 ) and (d) Shannon index (H0 ) for the
euphausiid community present in the study area. Triangulation with Linear Interpolation was used as a data gridding method in Surfer v.9 for S, J0 and H0 .

even earlier (e.g. Brinton, 1962; Antezana, 1978; see Brinton et al.,
2000) and changes may have occurred since then. On the other
hand, it has been recently proposed that the respiration rates and
oxidative stress in some euphausiid species like N. simplex can limit
and modulate their spatialtemporal variability in the Gulf of California, and this may explain the zoogeographic distribution patterns in this species (Tremblay et al., 2010). Based on
experimental evidence, Tremblay et al. (2010) postulate that N.
simplex does not inhabit regions with high temperature and low
oxygen concentrations, and exhibits high oxidative stress during
warm seasons. Following this point, it is likely that within a region
with oxygen decient waters, as occurs in the HCS (Escribano and
Schneider, 2007), this environmental variation might affect the
spatial and temporal distribution of this species in the HCS and
the study area. Also, the spatial and temporal distribution of zooplankton species is highly variable, at seasonal, inter-annual and
decadal scales (Brinton and Townsend, 2003), and changes could
occur within a 30 yr time period. Another potential source of
uncertainty, in terms of zoogeographical distribution, is the fact
that N. simplex has been considered to form two populations in
each hemisphere (Brinton, 1962, 1979; Brinton et al., 2000) but genetic analyses have not yet addressed this issue (J. Gmez-Gutirrez, personal communication).
The analysis of diversity patterns over spatial and temporal
scales is relevant to enhancing our knowledge of how biological
communities may respond to environmental changes forced by
large-scale variability (Beaugrand et al., 2002; Richardson and
Schoeman, 2004). In this sense, the pelagic marine ecosystem has
not yet received much attention (Gray, 2004), thus limiting our
baseline information for the assessment of potential changes in pelagic structure driven by climate change (Duffy and Stachowicz,
2006). Our work should, therefore, be considered as a contribution
that enhances our basic knowledge of the present community

structure of an important group of planktonic organisms in the

HCS.
In the context of environmental forcing on marine biodiversity,
cross-shelf gradients in the diversity indices of plankton communities have been reported from different regions of the world ocean
(Angel, 1993; Morgan et al., 2003; Gray, 2004; Gmez-Gutirrez
et al., 1995), and the general trend is for diversity to increase with
distance from the shore, accompanied by decreasing abundance
and, thus, a negative relationship between numerical abundance
and diversity can be found (Gray, 2004). This negative relationship
is also considered to be a more general attribute of plankton communities (Irigoien et al., 2004). The euphausiid community in our
study area also showed such patterns, as suggested previously by
Ayn et al. (2009) for the euphausiid community in the HCS. However, the high diversity and still higher abundance of euphausiids
in the oceanic region may deserve some further consideration given that euphausiids are indeed considered to be a low-diversity
group (Gibbons et al., 1999), possessing a total number of 86 species (Brinton et al., 2000). The number of species found in our study
accounted for about 26% of total described euphausiid species.
Furthermore, although abundances decreased towards offshore
zones, euphausiids were still well represented in all samples taken
during the study period. A potential line of explanation regarding
the high abundance and diversity of euphausiids over the entire
region may relate to an increased number of potential niches to
be occupied by species (Letessier et al., 2009). The coastal upwelling is clearly a highly heterogeneous environment, where mesoscale features over the horizontal plane, such as large eddies (see
Fig. 2), and probably strong vertical stratication and the presence
of coastal fronts and laments, may give rise to a variety of habitats
in the spatial domain, as suggested by Keister et al., (2009). This
spatial heterogeneity may also strongly interact with temporal
variation, mostly related to a seasonal cycle, as shown in our study

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R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Fig. 12. Size frequency distribution for the most frequent euphausiid species found in the study area separated by study zones. Observation numbers (n) are showed.

(see Figs. 611). In any case, in this region euphausiids constitute a

major food item for several commercially important sh such as
Jack Mackerel (Arancibia et al., 1995; Antezana, 2010) and Chilean
Hake (Cubillos et al., 2003). Therefore, the high abundance of euphausiids, cf. E. mucronata, may explain the high production of sh
biomass in the region, which gives rise to a large shery industry
(Arcos et al., 2001), as suggested by Antezana (2010).
In the context of the mechanisms and factors which regulate
euphausiid distribution, Siegel (2000) suggested the existence of
three different categories of factors that may control temporal
and spatial changes in krill distribution and abundance. Firstly,
the environmentalphysical factors that govern the physical environment of krill, such as temperature and mesoscale circulation
patterns either by creating boundaries for dispersion or by facilitating transport. Secondly, population dynamics parameters such
as growth, reproduction, recruitment and mortality. Lastly, species
behavior driven by horizontal or vertical migrations. All these fac-

tors on the whole will determine the krill abundance and distribution in a particular area. Our study however suggests that
upwelling events have some inuence on euphausiid species distribution and abundance. For example, our data suggest a strong
link between the observed distribution patterns of euphausiid species and environmental variables related to upwelling events (see
Table 5 and Fig. 14). In fact, E. mucronata, which is associated with
upwelling centers (Antezana, 1978; Escribano et al., 2000), show a
strong association with upwelling variability in the study area in
places where upwelling-favorable winds promote high food availability (phytoplankton), allowing the species to grow and reproduce, mainly in the CZ. Furthermore, the high abundance of
euphausiid eggs found in the CZ, which reects spawning locations, indicate a possible food-dependent cause for adult distribution. Similar patterns have been observed in other species
associated with upwelling events, such as E. pacica (Smiles and
Pearcy, 1971; Brinton, 1976).

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Some ecological advantages have been proposed in other

studies for the association between euphausiid abundance and
upwelling processes. For example, locations with strong subsurface upwelling usually have enhanced phytoplankton produc-

161

tivity and biomass in the overlying surface layer, which enhances food availability for the euphausiids when they migrate
up into the surface layer (Mackas et al., 1997). Another possibility, but not explored in this study, for adult aggregation in

Fig. 13. Dendrogram from cluster analysis for the species/samples matrix using the BrayCurtis similarity measure. White lines show nine statistically different clusters (ai)
(SIMPROF, p < 0.01). Dotted lines represent non-statistically different groups.

Fig. 14. Non-metric multidimensional scaling (NMDS) ordination of stations/samples based on species group abundance (ai) and environmental variability (vectors).
Stress = 0.08. CHLA, chlorophyll-a; SST, sea surface temperature; WIND_V, alongshore component of the wind.

162

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Fig. 15. Scatter-plot map of the association patterns among environmental gradients and euphausiid eggs and community predictors.

centers of upwelling is that the cross-shore zone of maximum

upward isopycnal displacement is also a zone of minimal
cross-shore pressure gradient, and hence minimal alongshore
transport by geostrophic currents.
Another interesting aspect in our study, is the higher abundance
of small individuals (<5 mm) in the OZ compared to the CZ, evidenced particularly in E. mucronata (Fig. 12), a predominantly neritic species. In light of this, observed patterns by Mackas et al.
(1991) and Lu et al. (2003) for E. pacica, among others, indicated
that the seaward surface layer ow would displace larvae and
juveniles offshore from both their hatch location and from the
center of the adult population. This is because the rate and
direction of the cross-shore transport vary with euphausiid body
size and developmental stage. For the non-migratory euphausiid
stages (nauplii, calyptopis and early furcilia), Ekman transport will
be a very important factor to consider. In contrast, for the later
diel-migratory stages (late furcilia through to adults), which
perform DVM, the dominant factor will be the shear velocity and
they will probably be exposed to transport that returns them to

the coastal area. Mesoscale structures such as eddies and

upwelling laments could have signicant implications for the
offshoreinshore transport and maintenance of euphausiid
populations by promoting favorable conditions in terms of food
and environment, as well as for sh, as suggested by CorreaRamrez et al. (2007, 2012) and Morales et al. (2007, 2010) in the
HCS and by Eden et al. (2009) and Govoni et al. (2010) for other regions. Certainly, this topic will require more attention in further
research.
Summarizing, our spatial and temporal analyses of species
abundances and community descriptors indeed show clear partitioning of the spatial and temporal habitats among species, and
therefore suggests that upwelling variation, which promotes high
heterogeneity and mesoscale structures, can be a key process in
maintaining the abundance and diversity of the euphausiid community. Finally, future and regular investigations will allow us to
further advance our understanding of the dynamics of, and the
ecological role played by, the euphausiid community in this
highly productive upwelling system.

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R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Table 5
Stepwise multiple regression of euphausiids abundance as a function of oceanographic and environmental variables in the study area along August 2007 and November 2008. An
analysis was applied at whole data obtaining a model for each environmental variable.

Model
r2
F-test
(fd, n  1)
P-value
SE
Species
Emuc
Egibbo
Erec
Nmeg
Ne
Sabr
Scar
Slon
Ssuh
Espi
Stages
Furcilia
Calyptopis
N+M
Eggs
Community
Predictor
S
N
J0
H0

LAT

LON

WU

WV

SST

CHLA

0.245
11.882
(16,585)
_***
2.521

0.422
21.218
(20,581)
_***
4.224

0.222
17.423
(11,311)
_***
3.264

0.124
14.500
(11,310)
_***
5.125

0.47
31.593
(16,570)
_***
1.640

0.263
14.325
(12,480)
_***
0.616

(+)***
()*

()***

()*
(+)*
(+)*
()*

(+)***

()*
(+)*
()***

(+)*
()***

(+)***

(+)***
(+)***

(+)***
()***

(+)**
(+)***
()*

(+)*

()*
()*
()***
(+)***

(+)**

()*

(+)*
(+)*

(+)*

()***
()**
(+)***

()***
(+)***
()*
()**

()***

(+)*

()***
()***
()*
(+)***

(+)*
(+)*
()*

N + M, nauplius plus metanauplius.

+ or  indicate positive or negative correlation, respectively. Non-signicant values are not indicated. LAT, latitude (S); LON, longitude (W); WU, zonal wind (m s1); WV,
meridional wind (m s1); SST, sea surface temperature (C); CHLA, chlorophyll-a (mg m3). Note: for LON, positive correlation is shoreward and, for LAT, positive correlation is
northward.
*
<0.05.
**
<0.001.
***
<0.0001.

Acknowledgements
This study was funded by projects of the Chilean Fishery
Research Funding, Grants FIP 2007-33 and FIP 2008-12. The
FONDAP-COPAS Center and Project FONDECYT 1080037 also provided support for eld studies. Three anonymous reviewers have
helped improving an earlier version of the work. The rst author
(R. R-B) thanks Jennifer Fisher, Cheryl Morgan (OSU/CIMRS) and Bill
Peterson (NOAA-NWFSC) to help with routines in PRIMER 6, valuable comments and discussion during his research stay (MECESUP
UCO0602 Fellowship) at Newport, OR, USA and also Jaime
Gmez-Gutirrez (CICIMAR, IPN, Mxico) made valuables comments on the manuscript. We add to the memory of Edward
Brinton (19242010) who passed away on January 13th. This work,
as well as many others in the world, would not have been possible
without the seminal work of Ed Brinton and his contribution to
euphausiid taxonomy, biogeography and population biology.

References
Alheit, J., Bernal, P., 1993. Effects of physical and biological changes on the biomass
yield of the Humboldt Current ecosystem. In: Sherman, K., Alexander, L.M.,
Gold, B.D. (Eds.), Large Marine Ecosystems. American Association for the
Advancement of Science Press, Washington, DC, pp. 5358.
Angel, M.V., 1993. Biodiversity of the pelagic ocean. Conservation Biology 7, 760
772.
Antezana, T., 1970. Eufusidos de la costa de Chile. Su rol en la economa del mar.
Revista de Biologa Marina 14 (2), 1927.
Antezana, T., 1976. Diversidad y equilibrio ecolgico en comunidades pelgicas. In:
Orrego, F. (Ed.), Preservacin del medio ambiente marino. Instituto de Estudios
Internacionales, Universidad de Chile, Santiago, pp. 4054.

Antezana, T., 1978. Distribution of euphausiids in the ChilePeru Current with

particular reference to the endemic Euphausia mucronata and the oxygen
minima layer. Ph.D. Thesis, University of California, San Diego, 489 pp.
Antezana, T., 1981. Zoogeography of euphausiids of the South Eastern Pacic Ocean.
In: UNESCO (Ed.), Memorias del Seminario sobre Indicadores Biolgicos del
Plancton. Montevideo, pp. 523.
Antezana, T., 2002. Vertical distribution and diel migration of Euphausia mucronata
in the oxygen minimum layer of the Humboldt Current. In: Frber Lorda, J. (Ed.),
Oceanography of the Eastern Pacic, vol. 2. Editorial CICESE, Mexico, pp. 1328.
Antezana, T., 2009. Species-specic patterns of diel migration into the oxygen
minimum zone by euphausiids in the Humboldt Current ecosystem. Progress in
Oceanography 83 (14), 228236.
Antezana, T., 2010. Euphausia mucronata: a keystone herbivore and prey in the
Humboldt Current System. Deep Sea Research Part II 57 (78), 652662.
Antezana, T., Aguirre, N., Bustamante, R., 1976. Clave ilustrada y distribucin
latitudinal de los eufusidos del Ocano Antrtico (Crustacea, Zooplancton).
Serie Cientica. Instituto Antartico Chileno 4, 5368.
Antezana, T., Melo, C., 2008. Larval development of Humboldt Current krill,
Euphausia mucronata G. O. Sars, 1883 (Malacostraca, Euphausiacea).
Crustaceana 81 (3), 305328.
Arancibia, H., Cubillos, L., Arcos, D., Grechina, A.S., Vilugrn, L., 1995. The shery of
horse mackerel (Trachurus symmetricus murphyi) in the south Pacic Ocean,
with notes on the shery off central-southern Chile. Scientia Marina 59 (34),
589596.
Arcos, D.F., Cubillos, L.A., Nuez, S.P., 2001. The jack mackerel shery and El Nio
199798 effects of Chile. Progress in Oceanography 49, 597617.
Ayn, P., Antezana, T., Escribano, R., Espinoza, P., 2009. Advances in the knowledge
on distribution and the ecological role of euphausiids in the Humboldt Current
System. In: 3rd GLOBEC Open Science Meeting. From Ecosystem Function to
Prediction. Victoria Conference Centre, Victoria, BC, Canada.
Baker, A.C., Boden, B.P., Brinton, E., 1990. A Practical Guide to the Euphausiids of the
World. Natural History Museum Publications, London, 96 pp.
Beaugrand, G., Reid, P.C., Ibanez, F., Lindley, J.A., Edwards, M., 2002. Reorganization of
North Atlantic marine copepod biodiversity and climate. Science 296, 16921694.
Brinton, E., 1962. The distribution of Pacic euphausiids. Bulletin of the Scripps
Institution of Oceanography 8, 51270.
Brinton, E., 1967. Vertical migration and avoidance capability of euphausiids in the
California Current. Limnology and Oceanography 12, 451483.

164

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Brinton, E., 1976. Population biology of Euphausia pacica off southern California.
Fishery Bulletin 74, 733762.
Brinton, E., 1979. Parameters relating to the distribution of planktonic organisms,
especially euphausiids in the Eastern Tropical Pacic. Progress in Oceanography
8, 125189.
Brinton, E., Townsend, A., 2003. Decadal variability in abundances of the dominant
euphausiid species in southern sectors of the California Current. Deep Sea
Research Part II 50 (1416), 24492472.
Brinton, E., Ohman, M.D., Townsend, A.W., Knight, M.D., Bridgeman, A.L., 2000.
Euphausiids of the World Ocean, Series: World Biodiversity Database CD-ROM
Series Window Version 1.0. Expert Center for Taxonomic Identication,
Amsterdam, Netherlands.
Clarke, K.R., Warwick, R.M., 2001. Change in Marine Communities: An Approach to
Statistical Analysis and Interpretation, second ed. Plymouth, PRIMER-E.
Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: User Manual/Tutorial. Plymouth,
PRIMER-E.
Correa-Ramrez, M.A., Hormazbal, S., Yuras, G., 2007. Mesoscale eddies and high
chlorophyll concentrations off central Chile (2939S). Geophysical Research
Letters 34, L12604. doi:10.1029/2007GL029541.
Correa-Ramrez, M.A., Hormazbal, S., Morales, C.E., 2012. Spatial patterns of annual
and interannual surface chlorophyll a variability in the Peru-Chile Current
System. Progress in Oceanography 92-95C, 817.
Cubillos, L.A., Rebolledo, H., Hernndez, A., 2003. Prey composition and estimation
of Q/B for the Chilean hake, Merluccius gayi (GadiformesMerluccidae), in the
central-south area off Chile (3440S). Archive of Fishery and Marine Research
50 (3), 271286.
Cury, P., Bakun, A., Crawford, R.J.M., Jarre, A., Quiones, R.A., Shannon, L.J., Verheye,
H.M., 2000. Small pelagics in upwelling systems: patterns of interaction and
structural changes in wasp-waist ecosystems. ICES Journal of Marine Science
57, 603618.
Daneri, G., Dellarossa, V., Quiones, R., Jacob, B., Montero, P., Ulloa, O., 2000. Primary
production and community respiration in the Humboldt Current System off
Chile and associated oceanic areas. Marine Ecology Progress Series 197, 4149.
Duffy, J.E., Stachowicz, J.J., 2006. Why biodiversity is important to oceanography:
potential roles of genetic, species, and trophic diversity in pelagic ecosystem
processes. Marine Ecology Progress Series 311, 179189.
Eden, B.R., Steinberg, D.K., Goldthwait, S.A., McGillicuddy, D.J., 2009. Zooplankton
community structure in a cyclonic and mode-water eddy in the Sargasso Sea.
Deep Sea Research Part I 56, 17571776.
Escribano, R., Hidalgo, P., 2000. Spatial distribution of copepods in the north of the
Humboldt Current region off Chile during coastal upwelling. Journal of the
Marine Biological Association (United Kingdom) 80 (2), 283290.
Escribano, R., Marn, V., Irribarren, C., 2000. Distribution of Euphausia mucronata at
the upwelling area of Peninsula Mejillones: the inuence of the oxygen
minimum layer. Scientia Marina 64, 6977.
Escribano, R., Schneider, W., 2007. The structure and functioning of the coastal
upwelling system off central/southern Chile. Progress in Oceanography 75,
343347.
Escribano, R., Hidalgo, P., Gonzlez, H.E., Giesecke, R., Riquelme-Bugueo, R.,
Manrquez, K., 2007. Seasonal and interannual variation of metazooplankton in
the coastal upwelling zone off central-southern Chile. Progress in
Oceanography 75, 470485.
Field, J.G., Clarke, K.R., Warwick, R.M., 1982. A practical strategy for analyzing
multispecies distribution patterns. Marine Ecology Progress Series 8, 3752.
Figueroa, D., Moffat, C., 2000. On the inuence of topography in the induction of
coastal upwelling along the Chilean coast. Geophysical Research Letters 27,
39053908.
Gibbons, M.J., Spiridinov, V., Tarling, G., 1999. Euphausiacea. In: Boltovskoy, D. (Ed.),
South Atlantic Zooplankton. Backhyus Publishers, Leiden, pp. 12411279.
Gmez-Gutirrez, J., Hernndez-Trujillo, S., Esqueda-Escarcega, G.M., 1995.
Community structure of euphausiids and copepods in the distribution areas
of pelagic sh larvae off the west coast of Baja California, Mexico. Scientia
Marina 59 (34), 381390.
Gmez-Gutirrez, J., Gonzlez-Chvez, G., Robinson, C.J., Arenas, F.V., 1999.
Latitudinal changes of euphausiid assemblages related to dynamics of the
scattering layer along Baja California, October 1994. Scientia Marina 63, 7991.
Gmez-Gutirrez, J., Peterson, W., Miller, C., 2005. Cross-shelf life-stage segregation
and community structure of the euphausiids off central Oregon (19701972).
Deep Sea Research Part II 52 (12), 289315.
Gonzlez, H.E., Daneri, G., Iriarte, J.L., Yannicelli, B., Menschel, E., Barra, C., Pantoja,
S., Lizrraga, L., 2009. Carbon uxes within the epipelagic zone of the Humboldt
Current System off Chile: the signicance of euphausiids and diatoms as key
functional groups for the biological pump. Progress in Oceanography 83 (14),
217227.
Govoni, J.J., Hare, J.A., Davenport, E.D., Chen, M.H., Marancik, K.E., 2010. Mesoscale
cyclonic eddies as larval sh habitat along the southeast United States shelf: a
Lagrangian description of the zooplankton community. ICES Journal of Marine
Science 67, 403411.
Gray, J.S., Aschan, M., Carr, M.R., Clarke, D.R., Green, R.H., Pearson, T.H., Rosenberg,
R., Warwick, R.M., 1988. Analysis of community attributes of the benthic
macrofauna of Frierfjord/Langesund fjord and in a mesocosm experiment.
Marine Ecology Progress Series 46, 151165.
Gray, J.S., 2004. Marine biodiversity: patterns, threats and conservation needs.
Biodiversity and Conservation 6, 153175.
Hormazabal, S., Nuez, S., Arcos, D., Espndola, F., Yuras, G., 2004. Mesoscale eddies
and pelagic sheries off central Chile. Gayana 68 (1), 291296.

Irigoien, X., Huisman, J., Harris, R.P., 2004. Global biodiversity patterns of marine
phytoplankton and zooplankton. Nature 429, 864867.
Keister, J.E., Peterson, W.T., Pierce, S.D., 2009. Zooplankton distribution and
cross-shelf transfer of carbon in an area of complex mesoscale circulation
in the northern California Current. Deep Sea Research Part I 56,
212231.
Kruskal, J.B., Wish, M., 1978. Multidimensional Scaling. Sage Publications, Beverly
Hills, CA.
Letelier, J., Pizarro, O., Nuez, S., 2009. Seasonal variability of coastal upwelling and
the upwelling front off central Chile. Journal of Geophysical Research 114,
C12009. doi:10.1029/2008JC005171.
Letessier, T., Cox, M., Brierley, A., 2009. Drivers of euphausiid species abundance and
numerical abundance in the Atlantic Ocean. Marine Biology 156 (12), 2539
2553.
Linacre, L., Palma, S., 2004. Variabilidad espacio-temporal de los eufusidos
frente a la costa de Concepcin, Chile. Investigaciones Marinas 32 (1), 19
32.
Lu, B., Mackas, D.L., Moore, D.F., 2003. Cross-shore separation of adult and juvenile
euphausiids in a shelf-break alongshore current. Progress in Oceanography 57,
381404.
Mackas, D.L., Washburn, L., Smith, S.L., 1991. Zooplankton community pattern
associated with a California Current cold lament. Journal of Geophysical
Research 96, 1478114797.
Mackas, D.L., Kieser, R., Saunders, M., Yelland, D.R., Brown, R.M., Moore, D.F., 1997.
Aggregation of euphausiids and Pacic hake (Merluccius productus) along the
outer continental shelf off Vancouver Island. Canadian Journal of Fisheries and
Aquatic Sciences 54, 20802096.
Mackas, D.L., Peterson, W.T., Zamon, J.E., 2004. Comparisons of interannual biomass
anomalies of zooplankton communities along the continental margins of British
Columbia and Oregon. Deep Sea Research Part II 51, 875896.
Mauchline, J., 1980. The biology of mysids and euphausiids. Advances in Marine
Biology 18, 373681.
Mauchline, J., Fisher, L., 1969. The biology of euphausiids. Advances in Marine
Biology 7, 154.
Montecino, V., Lange, C.B., 2009. The Humboldt Current System: ecosystem
components and processes, sheries, and sediment studies. Progress in
Oceanography 83 (14), 6579.
Montero, P., Daneri, G., Cuevas, L.A., Gonzlez, H.E., Jacob, B., Lizrraga, L., Menschel,
E., 2007. Productivity cycles in the coastal upwelling area off Concepcin: the
importance of diatoms and bacterioplankton in the organic carbon ux.
Progress in Oceanography 75, 518530.
Morales, C.E., Gonzlez, H.E., Hormazabal, S., Yuras, G., Letelier, J., Castro, L., 2007.
The distribution of chlorophyll-a and dominant planktonic components in the
coastal transition zone off Concepcin, central Chile, during different
oceanographic conditions. Progress in Oceanography 75, 452469.
Morales, C.E., Torreblanca, M.L., Hormazabal, S., Correa-Ramirez, M., Nuez, S.,
Hidalgo, P., 2010. Mesoscale structure of copepod assemblages in the coastal
transition zone and oceanic waters off central-southern Chile. Progress in
Oceanography 84 (34), 158173.
Morgan, C., Peterson, W.T., Emmett, R.L., 2003. Onshoreoffshore variations in
copepod community structure off the Oregon coast during the summer
upwelling season. Marine Ecology Progress Series 249, 223236.
Mujica, A., Pavez, C., 2008. Eufusidos de la zona central de Chile, archipilago Juan
Fernndez e islas Desventuradas. Latin American Journal of Aquatic Research 36
(2), 271282.
Neira, S., Arancibia, H., 2004. Trophic interactions and community structure in the
upwelling system off central Chile (3339S). Journal of Experimental Marine
Biology and Ecology 312 (2), 349366.
Neira, S., Arancibia, H., Cubillos, L., 2004. Comparative analysis of trophic structure
of commercial shery species off central Chile in 1992. Ecological Modelling
172 (24), 233248.
Palma, S., Silva, N., 2004. Distribution of siphonophores, chaetognaths, euphausiids
and oceanographic conditions in the fjords and channels of southern Chile.
Deep Sea Research Part II 51 (69), 513535.
Prez, M.J., Thomas, F., Uribe, F., Seplveda, M., Flores, M., Moraga, R., 2006. Fin
whales (Balaenoptera physalus) feeding on Euphausia mucronata in nearshore
waters off north-central Chile. Aquatic Mammals 32 (1), 109113.
Peterson, W.T., Miller, C.B., 1977. Seasonal cycle of zooplankton abundance and
species composition along the central Oregon coast. Fish B-NOAA 75 (4), 717
724.
Pillar, S.C., Stuart, V., Barange, M., Gibbons, M.J., 1992. Community structure and
trophic ecology of euphausiids in the Benguela ecosystem. South African Journal
of Marine Science 12, 393409.
Richardson, A.J., Schoeman, D., 2004. Climate impacts on plankton ecosystems in
the northeast Atlantic. Science 305, 16091612.
Shaw, W., Robinson, C.L.K., 1998. Night versus day abundance estimates of
zooplankton at two coastal stations in British Columbia, Canada. Marine
Ecology Progress Series 175, 143153.
Siegel, V., 2000. Krill (Euphausiacea) demography and variability in abundance and
distribution. Canadian Journal of Fisheries and Aquatic Sciences 57 (Suppl. 3),
151167.
Smiles, M.C., Pearcy, W.G., 1971. Size structure and growth rate of Euphausia pacica
off the Oregon coast. Fishery Bulletin 69, 7986.
Sobarzo, M., Djurfeldt, L., 2004. Coastal upwelling process on a continental shelf
limited by submarine canyons, Concepcin, central Chile. Journal of
Geophysical Research 109, C12012. doi:10.1029/2004JC002350.

R. Riquelme-Bugueo et al. / Progress in Oceanography 9295 (2012) 146165

Sobarzo, M., Bravo, L., Donoso, D., Garcs-Vargas, J., Schneider, W., 2007. Coastal
upwelling and seasonal cycles that inuence the water column over the
continental shelf off central Chile. Progress in Oceanography 75, 363382.
Sobarzo, M., Figueroa, D., Djurfeldt, L., 2001. Upwelling of subsurface water into the
rim of the Biobo submarine canyon as a response to surface winds. Continental
Shelf Research 21, 279299.
Strub, P.T., Mesias, J., Montecino, V., Rutllant, J., Salinas, S., 1998. Coastal ocean
circulation off western South America, Coastal Segment (6,E). In: Robinson, A.,
Brink, K. (Eds.), The Sea, vol. 11. Wiley, Hoboken, NJ, pp. 273313.
Thiel, M., Macaya, E., Acua, E., Arntz, W., Bastias, H., Brokordt, K., Camus, P., Castilla,
J.C., Castro, L.R., Corts, M., Dumont, C.P., Escribano, R., Fernndez, M.,
Lancellotti, D.A., Gajardo, J.A., Gaymer, C.F., Gmez, I., Gonzlez, A.E.,

165

Gonzlez, H.E., Haye, P.A., Illanes, J.-E., Iriarte, J.L., Luna-Jorquera, G., Luxoro,
C., Manrquez, P.H., Marn, V., Muoz, P., Navarrete, S.A., Prez, E., Poulin, E.,
Sellanes, J., Seplveda, A., Stotz, W., Tala, F., Thomas, A., Vargas, C.A., Vquez,
J.A., Vega, J.M.A., 2007. The Humboldt Current System of northern-central Chile.
Oceanographic processes, ecological interactions and socio-economic feedback.
Oceanography and Marine Biology 45, 195344.
Tremblay, N., Gmez-Gutirrez, J., Zenteno-Savn, T., Robinson, C.J., SnchezVelasco, L., 2010. Role of oxidative stress in seasonal and daily vertical
migration of three krill species in the Gulf of California. Limnology and
Oceanography 55 (6), 25702584.
Ware, D.M., Thomson, R.E., 2005. Bottom-up ecosystem trophic dynamics
determine sh production in the Northeast Pacic. Science 308, 12801284.