Deep-Sea Research II 57 (2010) 2089–2097

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Deep-Sea Research II
journal homepage: www.elsevier.com/locate/dsr2

Patterns of copepod diversity in the Chilean coastal upwelling system

Pamela Hidalgo 1,2, Ruben Escribano 2,3,n, Odette Vergara 3, Erika Jorquera 2,
Katty Donoso 3, Paula Mendoza 3
1
Instituto de Investigaciones Oceanológicas, Universidad de Antofagasta, P.O. Box 170, Antofagasta, Chile
2
Center for Oceanographic Research in the Eastern South Pacific (COPAS), University of Concepción, Chile
3
Department of Oceanography, University of Concepción, P.O. Box 160-C, Concepción, Chile

a r t i c l e in fo abstract

Article history: The copepod community structure from the Northern and Central/southern upwelling regions off Chile
Received 18 September 2010 was studied and compared. The derived community descriptors were species abundance (N), species
Accepted 18 September 2010 richness (R) and the Shannon-Wiener diversity index (H0 ). These descriptors were related to distinct
Available online 21 September 2010
habitats and conditions, sea surface temperature (SST) and depth of the upper boundary of the oxygen
Keywords: minimum zone (OMZ). From 159 samples, obtained between 2002 and 2008, a total number of 118
Biodiversity species were found of which the calanoids Paracalanus indicus, Acartia tonsa and Eucalanus inermis,
Copepods along with the cyclopoid Oithona similis, and the poecilostomatoids Triconia conifera and Oncaea media
Community structure were the dominant species. H0 was higher in the northern region, but no differences in N and R were
Coastal upwelling
detected between regions. N was higher in the epipelagic vs the deep habitat, but R and H0 did not differ.
Species richness
N, R and H0 correlated positively to SST and negatively to OMZ depth. The ascent of the OMZ to the
Oxygen minimum zone
Eastern South Pacific upper layer forced by upwelling was proposed as a mechanism that aggregates and increases copepod
Chile diversity in the food-rich photic zone. All these findings suggest a fundamental role of upwelling
Humboldt Current variation for modulating copepod dynamics and community structure in this highly productive but
strongly variable marine ecosystem.
& 2010 Elsevier Ltd. All rights reserved.

1. Introduction diversity from the Arctic to the tropics, although in the southern
hemisphere diversity seems high at high latitudes (Gray, 1997).
The study of biodiversity patterns is an important parameter in Except for few studies on biogeographic analyses of planktonic
understanding the processes structuring natural communities in systems (revised in Longhurst, 2006), these spatial patterns have
the marine environment. However, in the marine pelagic realm not been examined in the pelagic system
assessments of species diversity over spatial and temporal scales In addition to latitudinal and cross-shelf gradients, the
are rather scarce (Reid, 1992), compared to those performed in planktonic communities are also subjected to strong vertical
intertidal and benthic environments (e.g. Warwick and Clarke, gradients of most environmental variables and over rather short
2001; Gray, 1997). Biodiversity of pelagic communities is spatial scales. These gradients may exert a major impact on the
however recognized as a key issue for understanding the impact physiology, behavior and population demography of planktonic
of climatic changes on the functioning and structure of the global organisms, causing abrupt changes in vertical distribution,
marine ecosystems (Beaugrand et al., 2002; Hays et al., 2005; abundance, species composition and diversity of plankton over
Hooff and Peterson, 2006; Richardson, 2008). the vertical axis (Judkins, 1980; Wishner et al., 1998; Wishner
One of the relevant issues of marine biodiversity is related to et al., 2008; Escribano et al., 2009). Although vertical partitioning
spatial patterns of species and communities occurring over of plankton communities has been reported in some works
environmental gradients or contrasting habitats (Lawton, 1999; (e.g. Verheye et al., 1994; Irigoien and Harris, 2006), it has been
Hillebrand and Azovsky, 2001; Rex et al., 2001). For example, in difficult to identify and understand the underlying mechanisms
the benthic system diversity is greater in coasts than the open causing differential distributions over the vertical plane.
ocean, possibly because there is a greater range of habitats near The coastal upwelling system off Chile constitutes a large part
the coast (Gray, 1997). There is also a pattern of increasing of the Humboldt Current Systems recognized as one of the most
productive Large Marine Ecosystems of the world ocean (Sherman
et al., 1995). In this upwelling region, copepods and euphausiids
n dominate the zooplankton community and constitute the key link
Corresponding author at: Center for Oceanographic Research in the Eastern
South Pacific (COPAS), University of Concepción, Chile. for channeling primary production into fish production giving rise
E-mail address: [email protected] (R. Escribano). to a large fishery industry mainly based on small pelagic fishes

0967-0645/$ - see front matter & 2010 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dsr2.2010.09.012
2090 P. Hidalgo et al. / Deep-Sea Research II 57 (2010) 2089–2097

(Cushing, 1990). Studies on diversity of zooplankton are scarce in Mejillones 231 (85 m depth) were sampled during several
this region and the few works mostly deal with horizontal consecutive days (5–8 days) in the summers and winters 2005,
distribution (Heinrich, 1973; González and Marı́n, 1998; Escribano 2006 and 2007. In both sites, the samples were obtained in two
and Hidalgo, 2000; Linacre and Palma, 2004) and vertical depth strata with vertical tows of a 0.196 m2 opening mouth WP
distribution (Castro et al., 1993, Escribano et al., 2009) for limited net having a 200 mm mesh-size net.
taxa, or specific populations. Also, the coastal zone off Chile In the Central/southern region samples came from two
constitutes a highly heterogeneous and dynamic habitat over the sources. Firstly the COPAS Time Series Study off Concepción
horizontal plane, where zooplankton must cope with strong (Escribano and Schneider, 2007). In this study, zooplankton
gradients in temperature, density and food resources in addition samples were obtained monthly at the fixed Station 18 using a
to strong advective forces (Peterson, 1998; Marı́n et al., 2001; 200 mm mesh-size 1 m2 Tucker Trawl net towed obliquely at two
Giraldo et al., 2002). Over the vertical plane, in addition to a rather depth strata (0–50 m and 50–80 m). Details on sampling are
shallow thermocline (o50 m), the presence of the shallow provided in Escribano et al. (2007). For this work, we used only
oxygen minimum zone of the eastern south Pacific (Morales the samples obtained during 2002 and 2003, which have been
et al., 1999) causes a strong oxygen gradient near surface waters analyzed in detail for copepod composition. Monthly changes of
( o50 m) to which zooplankton must adapt, or avoid by remain- dominant copepod species (10% of total species) were previously
ing in the near-surface habitat (Escribano et al., 2009). All these assessed for the period 2002–2005 (Escribano et al., 2007), and for
selective pressures have probably influenced copepod evolution the period 2002–2008 the same dominant species were used to
in this type of upwelling system, but little is known on how such estimate interannual changes in copepod biomass (Escribano
forces affect biodiversity patterns. et al., submitted for publication). A second set of samples for this
Because of their abundance and occurrence, pelagic copepods southern region region came from the BIOZOO cruise carried out
have received more attention in the coastal upwelling zone off in winter 2008 at 5 stations over a cross-shelf transect from 5 to
Chile, in terms of population and community studies (Heinrich, 100 km offshore. At each station the same Hydrobios Multinet as
1973; Hidalgo and Escribano, 2001; Escribano et al., 2007), above was deployed to sample 4 strata down to 600 m at the
resulting in a considerable knowledge of species inhabiting the offshore station. In this case oblique tows were performed to
upwelling region. This information can now be used to derive some sample a greater volume of water ( 410 m3) because of lower
community descriptors and explore their relationships with copepod density in winter conditions.
environmental variability. In this work, we assess species diversity A total number of 159 samples were analyzed for this study,
of copepods in the coastal upwelling zone and examine the 107 samples were from the Northern region and 52 from the
influence of upwelling variation on copepod abundance Central/Southern zone. From these samples, all copepods were
and diversity. The work aims at understanding the impact identified to the species level (adults and copepodids, but not
of environmental variables on structuring planktonic communities nauplii) and counted, although some very dense samples were
in a highly productive and highly variable upwelling ecosystem. split with a Folsom splitter to count a maximum number of 200
individuals of a single dominant species.

2. Methods
2.3. Data analysis
2.1. The study area
All species were listed and their abundances expressed in
The coastal upwelling zone of Chile (Fig. 1) extends from 181S number per cubic meter. Data were thereafter divided into
to about 421S, i.e. nearly 2700 km of coast along the latitudinal categorical variables in according to their location and timing,
gradient. Because of different seasonal regimes of the upwelling such that they could be assigned to the following categories:
process, two major upwelling regions can be distinguished, (1) region (Northern, Central/Southern), year (6 levels), zone (inshore,
The northern upwelling region (181–301 S), and (2) the Central/ offshore), depth (above 100 m, deeper than 100 m), and season (4
southern upwelling region (301–421S). Both regions are known to seasons). The eventual effects of these factors were then tested on
represent key coastal upwelling systems supporting high primary derived community descriptors through unbalanced multifactor-
production rates (Daneri et al., 2000), strong fishery activity ial ANOVA. As community descriptors we derived total abundance
mostly based on small pelagic fishes (Alheit and Bernal, 1993; of copepods, species richness and the Shannon-Wiener index of
Arcos et al., 2001) and are subjected to strong interannual species diversity.
variability forced by the ENSO (El Niño southern oscillation) cycle In order to identify species assemblages or groups of species
(Escribano et al., 2004). related to each other a Cluster analysis was performed using the
correlation matrix and the Pearson correlation as a measure of
distance. This clustering analysis was applied only to a selected
2.2. Data sources group of species—the most abundant and recurrent ones. Two
environmental factors were available as indicator of upwelling
Locations of all sampling sites are illustrated in Fig. 1. For this conditions, the sea surface temperature (SST) and the upper
study, we used samples from northern Chile obtained during the boundary of the oxygen minimum zone (OMZ) considered as the
years 2005, 2006 and 2007. The first set of samples comes from depth of 1 mL O2 L  1 value of dissolved oxygen as defined in
the ZOMEI Cruise carried out between September and October other studies (Morales et al., 1999; Escribano et al., 2009). SST
2005 at two locations off 201S and 221S. We used the samples strongly correlates to upwelling intensity in this coastal system
from a single station at each site sampled day and night in 5 depth (Thomas et al., 2001; Sobarzo et al., 2007) and the OMZ depth
strata down to 700 m. All these samples were obtained with seems a key indicator of upwelling conditions in the coastal zone
vertical tows of a Hydrobios Midi-type multinet (0.25 m2 opening off Chile (Morales et al., 1999; Escribano et al., 2007). Both SST
mouth) equipped with five 200 mm mesh-size nets. A second set and OMZ were thus plotted and associated with the descriptors of
of samples came from the CENSOR (Climate Variability and the El the copepod community in order to examine the relationship
Niño Southern Oscillation) project through which two fixed between upwelling variation and the structure of the copepod
nearshore stations located off Chipana at 211S (90 m depth) and community.
 P. Hidalgo et al. / Deep-Sea Research II 57 (2010) 2089–2097 2091

Fig. 1. The Northern and Central/south upwelling regions off Chile in the eastern South Pacific, from illustrating locations of sampling stations from which zooplankton
samples were obtained 2002 to 2008 to analyze the copepod community.

3. Results 50
Northern upwelling region off Chile
P. indicus

3.1. Copepod composition

From a total number of 118 species identified from both

regions, it was found that some species may dominate the entire
coastal zone off Chile, and others are only present either in the
Northern or the Central/Southern region, or are rare in either of
C. brachiatus
RELATIVE ABUNDANCE (%)

T. conifera

O. media
A. tonsa

Corycaeus sp.
these regions (Fig. 2). It was also shown that in the Northern

E. inermis
O. similis

O. venusta

C. chilensis
C. typicus
region there are more dominant species, although some species,
O. nana

such as Calanoides patagoniensis, Oithona setigera, Drepanopus

forcipatus and Pleuromamma gracilis seem exclusive for the
0
Central/Southern region, while others such as Eucalanus inermis,

D. forcipatus
Oncaea venusta, Oithona nana and Centropages typicus were only

P. gracilis
O. setigera

found in the northern zone (Fig. 2).

C. patagoniensis

Table 2 lists all the species found and includes information on

preferential occurrence - northern or southern region, epipelagic or
deep water (4100 m), and coastal zone or offshore region. Most of
these species had been previously cited for Chile (e.g. Heinrich, 1973;
Hidalgo and Escribano, 2001). Calanoid copepods were the most
abundant and diverse from both regions. The calanoid Paracalanus
indicus was the most abundant and most recurrent species with 35%
of relative abundance and 96% of occurrence in all the samples. Central/southern upwelling region off Chile
Acartia tonsa was also very abundant with 7.8% of relative abundance
50
and 78% of occurrence. The large sized Eucalanus inermis was only
present in the northern region being rare in the Central/southern zone Fig. 2. Relative abundance of dominant copepods in two coastal upwelling zones
(4% of relative abundance and 53% of occurrence). The Cyclopoida off Chile illustrating their presence and dominance at each corresponding region.
order was well represented by the dominant Oithona similis with 14%
of relative abundance and 85% of occurrence. The Poecilostomatoida and distinct habitats are summarized in Table 2. Maximal
order was dominated by Oncaea media and Triconia conifera with 5% abundance of total copepods was ca. 40000 indiv. m  3 observed
and 6% of relative abundance, respectively. in a sample from spring 2005 from the northern region and
dominated by the small P. indicus, but the mean from all samples
was 761 indiv. m  3. In terms of species richness, the maximal
3.2. Community descriptors observed R in a single sample was 32 and it was found at Station
18 off Concepción in winter 2002, although the overall mean was
Estimated abundance of copepods (N), species richness (R) and about 14 species. The diversity index, H0 ranged between 0.03 and
the Shannon-Wiener biodiversity index (H0 ), separated by regions 1.15 with a grand mean of 0.66.
2092 P. Hidalgo et al. / Deep-Sea Research II 57 (2010) 2089–2097

Table 1
Summary of zooplankton sampling in the northern and southern upwelling regions of Chile to assess biodiversity and distribution of copepod species. Three different
sampling gears were used depending on cruises.

Year Season/Period Region/Cruise Net type Opening (m2) Towing Sampling depths (m)

2002 Monthly South Tucker 1 Oblique 0–50 m

(Station 18) Trawl 50–80 m
2003 Monthly South Tucker 1 Oblique 0–50 m
(Station 18) Trawl 50–80 m
2005 Winter North WP2 0.196 Vertical 0–90 m
(CENSOR) 0–85 m
2005 Spring North Multinet 0.25 Vertical 0–700 m
(ZOMEI) 5 depth strata
2006 Summer North WP2 0.196 Vertical 0–90 m
Winter CENSOR 0–85 m
2 depth strata
2007 Summer North WP2 0.196 Vertical 0–90 m
Winter CENSOR 0–85 m
2 depth strata
2008 Winter South Multinet 0.25 Horizontal 0–600
(BIOZOO) Oblique 5 depth strata

Biodiversity and total abundance of copepods are negatively positive relationship with SST (Fig. 5), indicating that warmer
related whereas there is a positive relationship between abun- water favored more copepods and increased diversity. Meantime,
dance and R (Fig. 3a, b). H0 and R correlated positively (Fig. 3c) N, R and H0 were all negatively correlated with OMZ depth (Fig. 6),
indicating that biodiversity is greater upon presence of more suggesting that copepods were more abundant and had higher
species. diversity when the OMZ became shallower.
To compare the community descriptors between regions a
one-way ANOVA was used after log-transformed data of N, R and
H0 . This was an unbalanced model of ANOVA since there were 4. Discussion
unequal sample sizes between regions (Table 3). This ANOVA
showed non-significant differences in N and R, but highly Although our data set provides information from two large
significant differences in the diversity index H0 (Table 4). upwelling regions and there is seasonal and interannual variation
Since samples came from different habitats or conditions, the involved in the data, there were different sampling methods
effect of these factors on the community descriptors could be and sampling gears, which may introduce some biases. Different
tested through a multifactorial analysis, assuming non- significant sampling depths might affect the copepod community being
interactions between factors. There were significant differences sampled considering the potential vertical partitioning of species
between epipelagic vs deep samples and among years for copepod in the upwelling zone (e.g. Judkins, 1980). In most cases however
abundances, significant seasonal and interannual effects on our sampling was concentrated in the upper 100 m where the
species richness, and no habitat/condition effects on species majority of copepod species aggregate in this upwelling zone due
diversity (Table 5). to constraints imposed by a shallow ( o200 m) oxygen minimum
zone (OMZ) (Escribano et al., 2009). Samples from deeper water
(4100 m) may have added some rare species adapted to inhabit
3.3. Community structure and environmental influences the OMZ, such as Eucalanus inermis (Hidalgo et al., 2005).
Although, this species tends to aggregate in the upper limit of
Community structure was examined using 27 species selected the OMZ in offshore water (ca. 200 m) and performs daily vertical
for their abundance and occurrence. These species showed migration to near the oxycline (ca. 60 m) (Hidalgo et al., 2005;
relative abundances greater than 0.5% and occurrences greater Escribano et al., 2009). Sampling gear might also affect the
than 5%. A cluster analysis was applied to the species matrix, community being sampled. In our case the mesh-size was the
using the Euclidean distance and the single linkage method. This same for all nets, but different opening diameter of the nets (see
analysis allowed the distinction of 5 groups of species or species Table 1) and towing speeds may be thought as influencing the
assemblages (Fig. 4). These assemblages reflected some distinc- copepods being captured. A comparison of MOCNESS net and WP2
tive faunistics groups. Group A, mainly represented by Clausoca- (Gjøsaeter et al., 2000) showed that even though total zooplank-
lanus arcuicornis and P. gracilis, appeared as offshore species, ton biomass does not differ between the nets, biomass of the large
rarely seen in the nearshore waters. Group B was dominated by size fraction ( 42000 mm) may be significantly higher in the
Calanus chilensis and well associated with upwelling centers. MOCNESS than in the WP2. This large size fraction however is
Group C represented species—typically E. inermis inhabiting the mostly represented by euphausiids and amphipods (Gjøsaeter
northern region and well related to the oxygen minimum zone. et al., 2000). Copepods species in the upwelling region of Chile are
Group D comprised of two species and appears as nearshore mostly comprised by small (0.5–1 mm in body length) and
species of the central/southern region. Finally, group E dominated medium size (1–3 mm in body length) individuals (Escribano
by P. indicus and A. tonsa clearly represented the dominant and et al., 2007), and it is unlikely that net avoidance can introduce
most widely spread species over the entire coastal zone (Fig. 4). large errors in abundance estimates.
Presence of distinctive faunistic groups suggested that pre- Sampling at different times of the year and over different time
vailing environmental conditions may influence the copepod scales may also influence the community being assessed. There
community structure. The two environmental variables used as are certainly seasonal fluctuations in species composition in this
indicators of upwelling conditions, SST and OMZ, were then upwelling zone (Hidalgo and Escribano, 2001; Escribano et al.,
related to the community descriptors. Abundance (N), species 2007) and this can explain the significant seasonal effects on
richness (R) and diversity (H0 ) all showed a weak, but significant species richness, although as suggested in previous studies
 P. Hidalgo et al. / Deep-Sea Research II 57 (2010) 2089–2097 2093

Table 2 Table 2. (continued )

List of species found in the coastal upwelling zone off Chile during 2002 and 2008.
Lucicutia grandis (Giesbrecht, 1895) Mecynocera clausi Thompson, 1888
CALANOIDA PARACALANIDAE (Nr, Co, De) (Nr-Sr, Co, Ep)
ACARTIIDAE Paracalanus indicus Wolfenden, 1905 Lucicutia simulans Sars, 1920 (Nr-Sr, PONTELLIDAE
(Nr-Sr, Co, Ep) Co, De)
Acartia tonsa Dana, 1849 (Nr-Sr, Co, Calocalanus styliremis Giesbrecht, 1888 Lucicutia flavicornis (Claus, 1863) (Nr- Pontellina plumata (Dana, 1849) (Nr-Sr,
Ep) (Sr, Co, Ep) Sr, Co, De) Co, Ep)
Acartia danae Giesbrecht, 1889 Calocalanus tenuis Farran, 1926 (Sr, Oc, Lucicutia sp. (Sr, Co, Ep) CYCLOPOIDA
(Nr,Co,Ep) Ep) TEMORIDAE OITHONIDAE
CALANIDAE Calocalanus sp. (Nr, Oc, Ep) Temora discaudata Giesbrecht, 1889 Oithona similis Claus, 1866 (Nr-Sr, Co,
Calanus chilensis Brodsky, 1959 (Nr-Sr, CENTROPAGIDAE (Nr-Sr, Co, Ep) Ep)
Co, Ep) Temora stylifera (Dana, 1849) (Nr-Sr, Oithona nana Giesbrecht, 1893 (Nr, Co,
Calanoides patagoniensis Brady, Centropages brachiatus (Dana, 1849) Co, Ep) Ep)
1883(Sr, Co, Ep) (Nr-Sr, Co, Ep) CANDACIIDAE Oithona setigera Dana, 1852(Sr, Oc, Ep)
Neocalanus gracilis (Dana, 1849) (Sr, Centropages typicus Kroyer, 1849 (Nr, Candacia bippinata Giesbrecht, 1889 Oithona plumifera Baird, 1843 (Nr-Sr,
Co, Ep) Co, Ep) (Nr-Sr, Co, Ep) Oc, Ep)
Neocalanus cristatus Kroyer, 1848 (Nr, EUCALANIDAE Candacia longimana Claus, 1863 (Nr- Oithona oculata Farran, 1913 (Nr, Co,
Oc, Ep) Sr, Co, Ep) Ep)
Neocalanus sp. (Sr, Co, Ep) Eucalanus inermis Giesbrecht, 1892 HETERORHABDIDAE Oithona sp. (Sr, Oc, Ep)
(Nr, Oc, De) Heterohabdus vipera (Giesbrecht, POECILOSTOMATOIDA
Mesocalanus tenuicornis (Dana, 1849) Eucalanus hyalinus (Claus, 1866) (Sr, 1889) (Sr, Co, Ep)
(Sr, Co, Ep) Oc, De) Heterorhabdus lobatus Bradford, ONCAEIDAE
Nannocalanus minor (Claus, 1863) (Nr- Eucalanus crassus Giesbrecht, 1888 1971(Nr-Sr, Co, Ep)
Sr, Oc, Ep) (Nr, Oc, De) Heterorhabdus spinifrons (Claus, 1863) Oncaea media Giesbrecht, 1891(Nr, Co,
METRIDINIDAE Subeucalanus subtenuis (Giesbrecht, (Nr-Sr, Co, Ep) Ep)
1888) (Nr, Oc, Ep) Heterorhabdus papilliger (Claus, 1863) Oncaea venusta Philippi, 1843 (Nr, Co,
Metridia lucens Boeck, 1864 (Nr-Sr, Oc, Subeucalanus longiceps (Matthews, (Sr, Co, Ep) Ep)
Ep) 1925) (Nr, Oc, Ep) Heterorhabdus sp. (Nr-Sr, Co, Ep) Oncaea mediterránea (Claus, 1863)
Metridia brevicauda Giesbrecht, 1889 RHINCALANIDAE (Nr-Sr, Co, Ep)
(Sr, Co, Ep) EUCHAETIDAE Oncaea sp. (Sr, Co, Ep)
Metridia gerlachei Giesbrecht, 1902 Rhincalanus nasutus Giesbrecht, 1888 Euchaeta marina (Prestandrea, 1833) Triconia antárctica (Heron, 1977) (Nr-
(Nr-Sr, Co, Ep) (Sr, Oc, Ep-De) (Nr-Sr, Co, De) Sr, Co, Ep)
Pleuromamma gracilis (Claus, 1863) SCOLECITRICHIDAE Euchaeta media Giesbrecht, 1888 (Nr- Triconia conifera (Giesbrecht, 1891)
(Sr, Oc, Ep) Sr, Co, Ep) (Nr-Sr, Co, Ep)
Pleuromamma abdominalis (Lubbock, Scolecithrix bradyi Giesbrecht, 1888 CORYCAEIDAE Microsetella rosea (Dana, 1848) (Nr-Sr,
1856) (Sr, Oc, Ep) (Nr-Sr, Co, Ep) Oc, Ep)
Pleuromamma quadrangulata (F. Dahl, Scolecithricella profunda (Giesbrecht, Corycaeus typicus (Kroyer, 1849) (Nr, Microsetella sp. (Nr, Oc, Ep)
1893) (Sr, Co, Ep) 1893) Co, Ep)
Metridia sp. (Nr, Oc, Ep) Scolecithricella ovata Farran, 1905 (Sr, Corycaeus flaccus (Giesbrecht, 1891) CLYTEMNESTRIDAE
Co, Ep) (Nr, Oc, Ep)
CLAUSOCALANIDAE Amallothrix emarginata (Farran, 1905) Corycaeus lautus Dana, 1849 (Nr-Sr, Clytemnestra rostrata (Brady, 1883)
(Nr, Co, Ep) Co, Ep) (Nr-Sr, Co, Ep)
Clausocalanus arcuicornis (Dana, 1849) Amallothrix sp. (Sr, Co, Ep) Corycaeus amazonicus Dahl F., 1894 SIPHONOSTOMATOIDA
(Sr, Oc, Ep) (Nr-Sr, Co, Ep)
Clausocalanus jobei Frost & Fleminger, Scaphocalanus elongatus Scott A., 1909 Coryceus speciosus Dana, 1849 (Nr-Sr, PONTOECIELLIDAE
1968 (Nr, Co, Ep) (Sr, Co, Ep) Co, Ep)
Clausocalanus sp. (Nr, Co, Ep) Scaphocalanus echinatus (Farran, 1905) Corycaeus sp. (Nr, Co, Ep) Pontoeciella abyssicola (Scott, 1893)
(Nr-Sr, Co, Ep) (Nr-Sr, Oc, De)
Ctenocalanus citer Heron & Bowman, Lophothrix frontalis Giesbrecht, 1895 Farranula sp. (Sr, Co, Ep)
1971 (Nr-Sr, Co, Ep) (Nr-Sr, Co, Ep) SAPPHIRINIDAE
Ctenocalanus vanus Giesbrecht, 1888 AETIDEIDAE Copilia sp. (Nr-Sr, Co, Ep)
(Nr-Sr, Co, Ep) Saphirina sp. (1) (Nr, Co, Ep)
Ctenocalanus sp. (Sr, Co, Ep) Aetideus armatus (Boeck, 1872) (Nr-Sr, Saphirina sp. (2) (Nr, Co, Ep)
Co, Ep) Sapphirella sp. (Sr, Co, Ep)
Microcalanus pygmaeus (Sars, 1900) Gaetanus miles Giesbrecht, 1888 (Nr- Vettoria granulosa Giesbrecht, 1891
(Sr, Co, Ep) Sr, Co, De) (Nr-Sr, Co, Ep)
Drepanopus forcipatus Giesbrecht, Gaetanus brevispinus Sars, 1900 (Nr-Sr, LUBBOCKIIDAE
1888 (Sr, Co, Ep) Co, De) Lubbockia squillimana Claus, 1863 (Nr-
Gaetanus teniuspinus Sars, 1900 (Nr Paraeuchaeta bradyi (With, 1815) (Nr- Sr, Co, Ep)
Co, De) Sr, Co, De) Lubbockia sp. (Sr, Co, Ep)
Gaetanus Krupii Giesbrecht, 1903 (Nr, Paraeuchaeta weberi Scott A., 1909 (Nr, MORMONILLOIDA
Co, De) Co, Ep) MORMONILLIDAE
Chiridius poppei Giesbrecht, 1893 (Nr- Paraeuchaeta scotti Farran, 1908 (Nr- Mormonilla phasma Giesbrecht, 1891
Sr, Co, Ep) Sr, Co, Ep) (Nr-Sr, Oc, De)
Chiridius gracilis Farran, 1908 (Nr-Sr, Paraeuchaeta sp. (Nr-Sr, Co, Ep) HARPACTICOIDA
Co, Ep) AEGISTHIDAE
Euchirella amoena Giesbrecht, 1888 AUGAPTILIDAE Aegisthus aculeatus Giesbrecht, 1891
(Nr-Sr, Co, Ep) (Sr, Oc, Ep)
Euchirella intermedia With, 1815 (Nr- Euaugaptilus magnus (Wolfenden, MIRACIIDAE
Sr, Co, Ep) 1904) Oculosetella gracilis Dana, 1849 (Sr, Oc,
Euchirella maxima Wolfenden, 1905 Haloptilus oxycephalus Giesbrecht, Ep)
(Sr, Co, Ep) 1898 (Nr-Sr, Co, Ep) ECTINOSOMATIDAE
Euchirella pulchra (Lubbock, 1856) PHAENNIDAE Microsetella norvegica (Boeck, 1865)
(Nr-Sr, Co, Ep) (Nr-Sr, Oc, Ep)
Euchirella bitumida With, 1915 (Nr-Sr, Phaenna spinifera Claus, 1863 (Nr-Sr,
Co, Ep) Co, Ep) Dominant habitats: Nr¼ Northern Region, Sr¼ Southern region, Co ¼coastal,
Euchirella sp. (Nr-Sr, Co, Ep) Onchocalanus subcristatus Wolfenden, Oc¼ Oceanic, Ep¼ Epipelagic, De ¼Deep.
1911 (Nr-Sr, Co, Ep)
LUCICUTIIDAE MECYNOCERIDAE
2094 P. Hidalgo et al. / Deep-Sea Research II 57 (2010) 2089–2097

Table 3
Abundance (N), species richness (R) and species diversity (H0 ) of copepods found in
1.4
the upwelling zone off Chile, as separated by regions and habitats. N ¼ number of
samples obtained during 2002 and 2008.
1.2
Region Habitat n N 7 SD (Number m  3) R H00
1.0
Northern Epipelagic/inshore 62 618.07 387.43 15.1 0.69
0.8 Epipelagic/offshore 20 2575.77 8934.28 11.4 0.71
H'

Deep/offshore 25 7.17 5.26 12.8 0.78

0.6

0.4 Southern Epipelagic/inshore 35 685.557 1156.48 14.2 0.53

Epipelagic/offshore 10 18.017 27.99 12.7 0.46
0.2 Deep/offshore 7 31.13 7 49.61 11.4 0.64
F1,155 =10.82, P=0.001
0.0
0 1 2 3 4 5
Loge (N) Table 4
One-way ANOVA to test regional differences in abundance (N) (number m  3),
species richness (R) and the Shannon-Wiener index of species diversity (H0 ) of
35 copepods found off Chile at two upwelling regions (pooled data) between 2002
and 2008.
30
Community Descriptor d.f F-ratio P
25
20 N 1 0.075 0.785
Error 155
15 R 1 0.002 0.961
R

Error 155
10 H 0
1 37.880 0.000**
Error 155
5
**
0 significant effects with P o0.05.
F1,155 =11.29, P=0.001

0 1 2 3 4 5
Table 5
Loge (N) Multifactorial ANOVA to test the effect of distinct habitats and conditions on the
community descriptors, abundance (N), species richness (R), and diversity index
(H0 ) of copepods found off Chile at two upwelling regions (pooled data) between
1.4 2002 and 2008.

1.2 Descriptor Habitat/Condition d.f. F-ratio P

1.0
N (number m  3) Inshore/offshore 1 2.463 0.119
0.8 Epipelagic/Deep 1 77.959 0.000**
Seasonal 3 1.289 0.280
H'

0.6 Year 5 3.942 0.002**

0.4 R Inshore/offshore 1 0.058 0.810

Epipelagic/Deep 1 2.132 0.146
0.2 Seasonal 3 8.356 0.000**
Year 5 24.439 0.000**
0.0
F1,155 =20.61, P=0.000
H0 Inshore/offshore 1 1.970 0.160
Epipelagic/Deep 1 3.063 0.088
0 5 10 15 20 25 30 35 Seasonal 3 0.886 0.456
R Year 5 0.518 0.599

Fig. 3. The relationships between community descriptors, abundance (N), species

richness (R) and Shannon-Wiener diversity index (H0 ) of the copepod pelagic
community from two coastal upwelling zones off Chile. All relationships are
year under the influence of cold and warm years caused by ENSO
significant and the broken lines represent 95% confidence limits.
(El Niño southern oscillation) (Escribano et al., 2004). This
possibility requires similar sampling schemes for every year
continuous reproduction year round in the upwelling zone of through the whole period. Escribano et al. (submitted for
dominant species (Escribano and McLaren, 1999; Hidalgo and publication) noted a negative trend in copepod biomass from
Escribano, 2007) may also explain the lack of seasonal effects on 2002 to 2008 in both regions and this was associated with a
total abundance and even on diversity. Because of different time gradual cooling from 2002 through 2008 with a greater intensity
scales of sampling in both regions, we cannot examine the of upwelling. It may thus be possible that alternate warm/cold
influence of different seasonal regimes of upwelling on commu- years can also impact copepod diversity.
nity structure, but it is likely that permanent upwelling in the Regarding the taxonomic composition, several species have an
Northern region (Strub et al., 1998; Thomas et al., 2001) may unclear taxonomic status, and possibly there are many species
allow a sustained and higher diversity in this zone, as compared that need to be clarified. Some families or genera may need
to the strongly seasonal regime of upwelling in the Central/ revision. Among the calanoids, Paracalanus indicus deserves some
southern region (Sobarzo et al., 2007). Meantime, significant special attention, because is clearly the dominant species in the
interannual variation in community descriptor may result from entire coastal zone off Chile and many times has been cited as
the usually strong variability in upwelling intensity from year to P. parvus, but our detailed morphological analysis following
 P. Hidalgo et al. / Deep-Sea Research II 57 (2010) 2089–2097 2095

Abundance (loge Number m-3)

Euclidean Distance
0.00 600.00 5

1
F1,155=9.19, P=0.0029
0
10 12 14 16 18 20 22
35
30
25
20
15

R
10
5
0 F1,157=4.609, P=0.033

10 12 14 16 18 20 22
1.4
1.2
1.0
H' 0.8
0.6
0.4
0.2
F1,155=22.947, P=0.000
0.0

10 12 14 16 18 20 22
SST (°C)

Fig. 5. The relationship between the community descriptors, abundance, species

richness (R) and Shannon-Wiener diversity index (H) and sea surface temperature
Fig. 4. Cluster analysis applied to the dominant species matrix of the pelagic (SST) of the pelagic community of copepods from two coastal upwelling zones off
community of copepods from two coastal upwelling zone off Chile (pooled data). Chile (pooled data). The relationships are all significant and dotted lines represent
the 95% confidence limits.

descriptions from Bowman (1971) and Bradford-Grieve (1994) When comparing the fauna between these regions we found
indicates the Chilean specimens closely resemble P. indicus. This common and exclusive species suggesting the presence of a
dominant species urgently needs to be revised, perhaps using gradual change in the community composition from north to
some molecular methods. Other species may also need some south. Also, despite similar abundances and richness the diversity
revision. Our work covered most species described for the coastal was significantly much higher in the northern region, suggesting a
zone, however, there are many species not included in this work latitudinal pattern of decreasing diversity from the north to the
that inhabit offshore regions in the area. We sampled as far as Polar region, at least down to the West Wind Drift zone (ca. 421S).
100 km from the coastline and assigned these samples to an This latitudinal pattern of diversity was also described for the
offshore habitat. Many other species are expected to be found in intertidal and benthic system of the Chilean coast (Fernández
the oceanic region ( 4100 km from the coast) (Heinrich, 1973). et al., 2000). This pattern of latitudinal decrease may also
Our work covered only coastal upwelling zone, or the coastal zone correspond with the negative trend in diversity from equatorial
under the influence of coastal upwelling, which may reach up to to polar region which has been matter of many analyses (Angel,
100–150 km from the shore (Strub et al., 1998). 1993; Duffy and Stachowicz, 2006).
An important issue regarding spatial patterns of diversity The influence of habitat/condition on community descriptors
involves latitudinal gradients (Angel, 1993). The Chilean upwel- should also be taken into account to explain observed patterns of
ling zone is subjected to a strong latitudinal gradient reflected in the copepod community. Decreased abundance of copepods in
almost all oceanographic variables from warm equatorial/sub- deeper water compared to the upper ( o100 m) layer is not
tropical to cold subantarctic waters (see Strub et al., 1998). surprising and the strong oxygen gradient may be a major factor
Dominant fauna in the whole region must therefore be influenced affecting copepod abundance in depth in the region (Judkins,
by equatorial species in the northern region and Polar/subantarc- 1980; Escribano et al., 2009). It is relevant to show that R and H0
tic species in the Central/southern region, and possibly a can be maintained in deeper water revealing the high capacity of
transition zone located around the 301S corresponding to the copepods to adapt and inhabit apparently hostile environments
tropical convergence. These biogeographic patterns can be (low food, low oxygen) (Escribano et al., 2009). It is important to
assigned to the Pacific biome according to Longhurst (2006) and note the positive relation between community descriptors and
were suggested by Escribano et al. (2003) in relation to pelagic temperature. At least in the northern region off Chile, copepod
species. Our samples however were not distributed over the abundance seems to positively respond to temperature (Ulloa
latitudinal gradient, but they simply represented two regions. et al., 2001) suggesting this environmental variable as a driving
2096 P. Hidalgo et al. / Deep-Sea Research II 57 (2010) 2089–2097

5 Acknowledgments
Abundance (loge Number m-3)

4
Funding for obtaining samples and data for this work has been
3 provided by COPAS FONDAP Center, CENSOR Project of the EUC,
and FONDECYT 1080037 project. Data processing and integration
2 has been carried out in the framework of OBIS (Ocean Biogeo-
graphic Information System) of Census of Marine Life Program
1
(CoML) through the Eastern South Pacific RON (ESPOBIS). This
F1,155=18.865, P=0.000
0 work is a contribution to the international program Census of
0 20 40 60 80 100 120 140 160 180 200 Marine Zooplankton (CMarZ) of CoML.
35
30
25
20 References
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