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Trophic structure in the northern Humboldt Current system: new

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DOI: 10.1007/s00227-017-3119-8

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Mar Biol (2017) 164:86
DOI 10.1007/s00227-017-3119-8

ORIGINAL PAPER

Trophic structure in the northern Humboldt Current system: new

perspectives from stable isotope analysis
Pepe Espinoza1,2 · Anne Lorrain3   · Frédéric Ménard4 · Yves Cherel5 · Laura Tremblay‑Boyer6 · Juan Argüelles1 ·
Ricardo Tafur1 · Sophie Bertrand2 · Yann Tremblay2 · Patricia Ayón1 · J.‑M. Munaron3 · Pierre Richard7 ·
Arnaud Bertrand2 

Received: 19 April 2016 / Accepted: 1 March 2017

© Springer-Verlag Berlin Heidelberg 2017

Abstract The northern Humboldt Current system
(NHCS) is the most productive eastern boundary upwelling
system (EBUS) in terms of fish productivity despite hav-
ing a moderate primary production compared with other
EBUS. To understand this apparent paradox, an updated
vision of the trophic relationships in the NHCS is required.
Using δ13C and δ15N as a proxy of foraging habitat and
trophic position, respectively, we focused on thirteen rel-
evant taxonomic groups from zooplankton to air-breath-
ing top predators collected off Peru from 2008 to 2011.
Responsible Editor: C. Harrod.
Reviewed by A. Malzahn and undisclosed experts.
Electronic supplementary material  The online version of this
article (doi:10.1007/s00227-017-3119-8) contains supplementary
material, which is available to authorized users.
* Anne Lorrain
anne.lorrain@ird.fr
1
Instituto del Mar del Perú, Esquina Gamarra y Gral. Valle
s/n, Apartado 22 Callao, Lima, Peru
2
IRD, UMR248 MARBEC IRD/IFREMER/UM/CNRS,
Avenue Jean Monnet, CS 30171, 34203 Sète Cedex, France
3 covers less than 0.1% of the World Ocean surface but sus-
IRD, LEMAR UMR 6539 IFREMER/IRD/CNRS/UBO,
Technopole Brest Iroise, 29280 Plouzané, France
4 NHCS is driven by bottom-up forcing at local (Bertrand
Aix Marseille Univ, Université de Toulon, CNRS, IRD, MIO,
Marseille, France
5 et al. 2016), interannual (Barber and Chavez 1983), multi-
Centre d’Études Biologiques de Chizé (CEBC), UMR 7372
du CNRS-Université de La Rochelle, 79360 Villiers‑en‑bois,
France
6
Secretariat of the Pacific Community, SPC, BP D5,
98848 Nouméa Cedex, New Caledonia
7
Littoral, Environnement et Sociétés, UMR 7266 CNRS-
Université de La Rochelle, 17042 La Rochelle, France
Estimates of trophic position (TP) for the anchoveta
Engraulis ringens were high (3.4–3.7), in accordance with
previous studies showing zooplankton as a major contribu-
tor to anchoveta diet and challenging the often-cited short
food chain hypothesis for this ecosystem. The squat lobster,
Pleuroncodes monodon, a little studied consumer had simi-
lar δ15N values that of anchoveta, and thus similar trophic
position. However, their differing δ13C values indicate that
their foraging habitat do not fully overlap, which could alle-
viate potential competition between these species. Given
the current high biomass of squat lobsters in the ecosys-
tem, we encourage that future research focus on this spe-
cies and its role in the diet of top predators. The present
study provides first estimates of the relative TP of impor-
tant taxonomic groups in the NHCS, which are needed to
revisit anchoveta-centred ecosystem models for this region.
Further work using amino acid compound specific sta-
ble isotope analyses is now required to confirm these TP
estimates.
Introduction
The northern Humboldt Current system (NHCS) off Peru
tains ~10% of the world fish catch (Chavez et al. 2008). The
et  al. 2014), intraseasonal (Bertrand et  al. 2008b; Passuni
decadal (Ayón et  al. 2008a) and centennial to millennial
time scales (Gutiérrez et  al. 2009; Salvatecci 2013). It is
the most productive ecosystem in terms of fish production,
but it generates a moderate primary production compared
with other eastern boundary upwelling systems (EBUSs)
(Bakun and Weeks 2008; Chavez et al. 2008).

13
Vol.:(0123456789)
 86   Page 2 of 15
A variety of works have focused on this apparent para-
dox (e.g. Bakun and Broad 2008; Chavez and Messié 2009;
Bertrand et al. 2011; Brochier et al. 2011). However, fully
understanding the processes in play and the energetic fluxes
requires a comprehensive vision of actual trophic relation-
ships. Indeed, Espinoza and Bertrand (2008, 2014) and
Espinoza et al. (2009) showed that the Peruvian anchovy or
anchoveta Engraulis ringens forage mainly on zooplankton,
refuting the prevalent short food chain hypothesis that pos-
its that anchoveta feed directly on diatoms (Ryther 1969;
Pauly et al. 1989). Their results suggest an ecological role
for forage fish that challenges current trophic models for
the NHCS where forage fish rely almost exclusively on
diatoms. In the NHCS, the socioeconomic role of forage
fish resulted in anchoveta-centered models of the Peruvian
ecosystem (e.g., Pauly and Tsukayama 1987; Muck 1989).
However, other organisms can potentially play an impor-
tant ecological role in this system. For example, the squat
lobster Pleuroncodes monodon, which inhabits pelagic
habitats in the NHCS, is particularly abundant since the
mid-1990s (acoustic estimates range from 0.6 to 3.4  mil-
lion tonnes; Gutiérrez et  al. 2008), and is a potentially
important prey for seabirds, mammals and coastal fish
(Arias-Schereiber 1996; Jahncke et al. 1997). Since the dis-
tribution of anchoveta and squat lobster overlap along the
Peruvian coast (Gutiérrez et al. 2008), they could compete
for food or predate on each other. However, squat lobsters
have seldom been observed in anchoveta stomachs.
The question of P. monodon’s potential role as prey to
apex predators, such as fur seals and seabirds, as well as
anchoveta is, therefore, still under debate, and central to
understand the trophic functioning of the NHCS. Another
key species in the ecosystem is the jumbo squid Dosidicus
gigas, which is exploited by an important fishery. While
stomach content and stable isotope analyses have improved
our understanding of this species’ habitat, life-history and
resource use (Lorrain et  al. 2011; Argüelles et  al. 2012;
Alegre et  al. 2014), a comprehensive picture of its actual
role within the NCSH foodweb is still lacking.
An updated vision of the trophic relationships in the
NHCS is thus required, and must be extended to species
beyond anchoveta. Previous trophic studies relied solely
on stomach content analysis (e.g., Espinoza and Bertrand
2008; Alegre et  al. 2014, 2015). This method has limita-
tions since it is logistically difficult to apply for a wide suite
of species; it underestimates the importance of soft bodied,
rapidly digested or unidentifiable food items (Tieszen et al.
1983), and it only provides a snapshot in time of ingested
prey items (Olson et al. 2010). In contrast to stomach con-
tent analysis, the stable isotope analysis of consumer tis-
sues integrates dietary information over extended periods
and has been proved to be a powerful tool to study the
trophic ecology of marine organisms at the ecosystem scale
13
Mar Biol (2017) 164:86
(Hobson et al. 2002). The δ13C values, which only increase
slightly between diet and a consumer (Post 2002), are gen-
erally used as a tracer of the habitat or the feeding zone
while δ15N values are used as an indicator of the trophic
position of consumers (Cherel and Hobson 2007). How-
ever, the δ13C and δ15N values at the base of the food web
can have a high spatial variability (Vander Zanden and Ras-
mussen 1999). These geographical variations in the stable
isotope values of primary producers (also called δ13C and
δ15N baselines) have been shown to propagate up the food
web and are reflected in the isotope value of organisms,
including top predators (Olson et  al. 2010; Graham et  al.
2010). An assessment of isotopic baselines is, therefore,
required for the accurate estimation of a consumer’s trophic
position. A prominent feature of the NHCS is the pres-
ence of a shallow (25–50  m) permanent OMZ along the
coast (Fuenzalida et al. 2009; Bertrand et al. 2010), which
strongly affects marine life (Bertrand et  al. 2008a, 2011,
2014) and hence trophic interactions. In this OMZ, in par-
ticular south of ~7.5°S where the upper limit of the OMZ
is shallow (Bertrand et al. 2010; Mollier-Vogel et al. 2012),
both intense denitrification and anaerobic ammonium oxi-
dation (anammox) occur (Lam et  al. 2009). These high
intensities of denitrification and anammox in the southern
areas of the NHCS led to a strong latitudinal gradient with
higher baseline δ15N values in the southern areas rela-
tive to northern areas as already shown by Argüelles et al.
(2012) and Mollier-Vogel et al. (2012). In addition to these
latitudinal effects on δ15N values in the NHCS, size-based
effects have also been shown as important factors in the
jumbo squid δ15N values (Argüelles et al. 2012) and must
also be accounted for in the NHCS.
Within this context, the main objective of this study
was to estimate the trophic position of different taxonomic
groups, important in terms of biomass or fisheries in the
NHCS and spanning a large TP range. For that purpose
we analyzed the δ13C and δ15N values of 13 key groups
of organisms collected off Peru from 2008 to 2011, with
particular attention to body length and latitudinal effects.
The selected groups, which can be individuals species or
broader taxonomic groups are: (1) copepods, euphausi-
ids and squat lobster for the crustacean zooplankton com-
partment; (2) the mesopelagic fishes myctophids and
Vincinguerria lucetia; (3) the pelagic fish anchoveta,
mackerel (Scomber japonicus) and jack mackerel (Tra-
churus murphyi), (4) the demersal hake (Merluccius gayi
peruanus); (5) the jumbo squid; (6) two seabirds species,
namely the Peruvian booby (Sula variegata) and the Gua-
nay cormorant (Phalacrocorax bougainvillii); and (7) the
South American fur seal (Arctocephalus australis). Based
on δ13C and δ15N values and the resulting estimations
of trophic positions for these 13 groups, we provide new
insights on the functioning of the NHCS foodweb.
Mar Biol (2017) 164:86 Page 3 of 15  86
Materials and methods
Sampling
Collection samples covered most of the latitudinal range
of the Peruvian coast in the NHCS (Table  1; Fig.  1,
03°3′–18°0  S). Zooplankton, fish and squid samples
were collected from 2008 to 2011 during routine acous-
tic surveys performed by the Peruvian Institute of the Sea
(IMARPE) (Table  1). Fish and squids were measured for
standard or mantle length (mm), respectively. In large
individuals, a small piece (1 × 1 cm) of the anterior dorsal
muscle was collected. In small fish, the head, gut, and cau-
dal fin were removed, and the remaining whole body was
collected. Euphausiids and copepods were analyzed as a
whole. For squat lobsters, carapace length was measured,
the telson was dissected and the exoskeleton was removed
to sort the internal muscle. All samples were stored fro-
zen and processed later in the laboratory, except for jumbo
squid samples which were stored in 70% ethanol. Seabird
and fur seal blood were collected via venipuncture. Blood
samples were first stored in 70% ethanol in the field and
then at −20 °C until analysis. Storage in 70% ethanol does
not alter the bulk δ15N values of blood (Hobson et al. 1997)
or squid mantle tissue (Ruiz-Cooley et al. 2011), but some
studies report a slight increase in bulk δ13C values (Bugoni
et al. 2008).
Samples preparation and analysis
Jumbo squid samples were freeze dried for 48  h. All
other samples were dried in an oven at 60 °C for 48  h.
They were then ground to a fine powder. Lipid extrac-
tion was performed on muscle samples using 20  ml of
cyclohexane on powder aliquots of about 1 g. Lipid free
samples were dried at 60 °C before processing. Lipids
were not removed from seabird and fur seal blood sam-
ples, as the low lipid content of whole blood does not
require lipid extraction prior to isotopic analysis (Cherel
et  al. 2005). Carbonates were also removed for copep-
ods and euphausiids by soaking them in diluted HCl
for 5  min (Jacob et  al. 2005). Samples (~300  µg) were
analyzed using an elemental analyzer (Flash EA1112,
Thermo Scientific, Milan, Italy) coupled to an isotope
ratio mass spectrometer (Delta V Advantage with a
Conflo IV interface, Thermo Scientific, Bremen, Ger-
many). Results were expressed according to interna-
tional standards (Vienna Pee Dee Belemnite for δ13C
and ­N2 in air for δ15N) following the formula: δ13C or
δ15N=­[(Rsample/Rstandard)  −  1] × 103 (in‰), where R is
13 12
C/ C or 15N/14N. Reference gas calibration was done
using reference materials (USGS-24, IAEA-CH6, IAEA-
600 for carbon; IAEA-N1, -N2, -N3, -600 for nitrogen).
Analytical precision based on isotope values of acetani-
lide (Thermo Scientific) was <0.15‰ both for δ13C and
δ15N measurements. Values are means ± SD.
Statistical analysis
The different sources of variability driving the values of
δ15N between taxa, specifically, size and latitude (Ménard
et al. 2007; Décima et al. 2013; Lorrain et al. 2015) were
explored with linear mixed-effects (LME) models (Pin-
heiro and Bates 2000), which are robust to unbalanced
sampling schemes like the one we have here. In this eco-
system δ15N values vary significantly with both size and
latitude (Argüelles et al. 2012), and the use of LME mod-
els optimizes the information used to account for the effect
of these two variables in the predicted values of δ15N. The
resulting standardized predictions allow the comparison of
δ15N values across different species.
LME allowed us to combine a random-effects analysis
of variance model (variability amongst species) with linear
regression models. The taxon effect was treated as a ran-
dom variation around a population mean, while the covari-
ates of interest, body length and latitude, were assessed as
two continuous covariates. The LME population estimates
of δ15N values for the different groups were then further
used to estimate trophic positions (TP). Different mod-
els were performed with latitude and body length added
sequentially as fixed effects or as random effects with spe-
cies. These models were tested using Akaike criterion fol-
lowing Symonds and Moussalli (2011) and key model
selection results are summarised in Table S1. The assump-
tion of normality and independence for the random effect
and the residuals were graphically assessed (not shown).
The fitted coefficients for the selected best models are
shown in Table S2. Population predicted δ15N values using
the most parsimonious models were computed and used as
surrogates of the trophic positions of the different species
in the range of the corresponding observed body lengths for
the fixed latitudes, or in the range of the observed latitudes
for a fixed body length (Table 2). We note that inter-annual
variations could affect our results, but we were not able to
include a year effect in the final analysis because some spe-
cies were only observed on specific years and/or locations,
such that the year effect would have been confounded with
those other covariates.
A preliminary scrutinizing of the data showed a shift in
δ15N at ~7.5°S coherent with the impact of the OMZ on
baseline δ15N values (Argüelles et al. 2012; Mollier-Vogel
et  al. 2012). Indeed, along the Peruvian coast, the OMZ
get more intense and shallow south of ~ 7.5°S (Fuenzalida
et al. 2009; Bertrand et al. 2010). Accordingly, we split our
dataset and constructed different models north and south of
7.5°S. We then predicted the δ15N values within each zone
13
 86  

13
Page 4 of 15

Table 1  Data description
Species Code Year range Storage Sample n Body length Latitudinal range (°S) Longitudinal range (°W) δ13C δ15N C:N
range (mm) mean ± SD mean ± SD mean ± SD

Invertebrates
 Copepods Copepod 2008–2010 Frozen Whole body 33 3.85–14.65 76.07–83.57 −20.3 ± 1.3 7.6 ± 1.3 4.8 ± 0.6
 Euphausiids Euph 2008–2011 Frozen Whole body 17 19–24 3.85–14.65 76.07–81.87 −18.1 ± 0.9 8.8 ± 0.6 3.9 ± 0.2
 Pleuroncodes monodon SLobst 2008–2011 Frozen Muscle tissue 43 8–22.9 4.42–12.43 77.35–81.55 −15.2 ± 0.4 13.3 ± 1.2 3.9 ± 0.2
 Dosidicus gigas JSquid 2008–2011 Alcohol Muscle tissue 337 20–988 3.48–18.32 71.12–84.25 −17.1 ± 0.9 13.4 ± 3.4 3.2 ± 0.1
Fish
 Myctophids Myct 2008–2010 Frozen Muscle tissue 35 35–100 5.25–7.33 81.40–83.57 −19.0 ± 1.0 9.0 ± 1.2 3.4 ± 0.3
 Vinciguerria lucetia Vincig 2008–2011 Frozen Muscle tissue 23 32–65 5.25–15.05 80.25–83.57 −18.5 ± 0.6 10.7 ± 2.8 3.4 ± 0.1
 Engraulis ringens Anch 2008 Frozen Muscle tissue 165 31–165 4.42–16.02 74.47–82.25 −16.3 ± 1.2 12.1 ± 2.3 3.3 ± 0.1
 Scomber japonicus Mackerel 2008–2011 Frozen Muscle tissue 8 32–230 5.25–15.85 76.15–82.25 −17.6 ± 1.7 11.8 ± 3.3 3.2 ± 0.1
 Trachurus murphyi JM 2008–2011 Frozen Muscle tissue 14 118–310 4.42–15.85 76.15–81.55 −17.2 ± 0.6 17.5 ± 2.9 3.2 ± 0.0
 Merluccius gayi peruanus Hake 2008 Frozen Muscle tissue 84 100–480 3.70–7.47 80.28–81.38 −16.3 ± 0.6 11.4 ± 0.5 3.2 ± 0.1
Marine birds and mammals
 Sula variegata Booby 2009–2010 Alcohol Blood 37 nd 11.75 77.47 −14.7 ± 0.2 14.7 ± 0.2 3.3 ± 0.0
 Phalacrocorax bougainvillii Guanay 2009–2010 Alcohol Blood 37 nd 11.75 77.47 −15.0 ± 0.2 15.1 ± 0.2 3.3 ± 0.1
 Arctocephalus australis Fur seal 2010 Alcohol Blood 16 1200–1490 15.37 75.18 −16.9 ± 0.3 18.3 ± 0.4 3.5 ± 0.0
Mar Biol (2017) 164:86
Mar Biol (2017) 164:86 Page 5 of 15  86

Fig. 1  Sampling stations off Peru

Table 2  Predicted δ15N (‰) Species Fixed body Predicted δ15N Predicted TP Predicted δ15N Predicted
values and trophic position (TP) size (mm) at 7.0°S at 7.0°S at 11.7°S TP at
at 7.0°S and 11.7°S 11.7°S

Copepods 1 7.8 2.5a 9.5 2.5a

Euphausiids 2 8.8 2.8
Myctophids 50 9.1 2.9
Vinciguerria lucetia 50 9.2 2.9 12.6 3.4
Mackerel 200 11.4 3.6 12.4 3.3
Anchoveta 140 10.9 3.4 13.7 3.7
Squat lobster 20 11.8 3.7 13.6 3.7
Jumbo squid 400 11.1 3.5 14.3 3.9
Hake 280 11.5 3.6
Jack mackerel 250 15.1 4.2
Peruvian booby 400 14.6 4.5
Guanay cormorant 400 15.0 4.6
South American Fur seal 1300 16.0 4.9
a
 Assumed

at the latitude where the greatest number of sampled spe- Trophic position estimates
cies overlapped, i.e. at 11.7°S for the southern zone and at
7.0°S for the northern zone. For comparison purposes with literature data, we estimated
absolute TP values based on predicted δ15N values at 7.0°S

13
 86   Page 6 of 15 Mar Biol (2017) 164:86

and 11.7°S. These estimates necessarily rely on several

assumptions inherent to any stable isotope study that will
be detailed in the “Discussion” section. These assumptions
are (1) the use of a fixed discrimination factor for all spe-
cies while variable isotopic discrimination factors between
predator and prey groups have been shown according to
diet quality or position in the food web (Caut et  al. 2009;
Hussey et al. 2014); (2) the use of a pelagic baseline unique
between years and for both benthic and pelagic species and
(3) the value of the baseline TP. These TP were estimated
using the following equation (Post 2002):
TPconsumer = 𝛾baseline + 𝛿 15 Nconsumer −𝛿 15 Nbaseline ∕Δ15 N
[( ) ]

where δ15Nconsumer is the δ15N value of the consumer,

δ15Nbaseline is the δ15N value of the baseline, γbaseline is the
trophic position of the organism used to establish baseline,
and Δ15N is the 15N discrimination factor, i.e., the enrich-
ment in 15N per trophic level (Vander Zanden et al. 1997;
Post 2002). We used (1) a mean 15N discrimination factor
of 3.4‰ as the average 15N enrichment between the mus-
cle of marine fishes and invertebrates, and (2) copepods as
primary consumers. The sampled copepods were mostly
large species, i.e. Eucalanus spp. and Centropages spp. that
are known to be omnivorous feeders (Boyd et al. 1980). We
Fig. 2  δ13C vs. δ15N biplot for zooplankton, nekton and top predators
thus assumed γ = 2.5 for copepods as in Olson et al. (2010). collected in the NHCS. Values are ± SD
15
N discrimination factor can vary with prey and predator
tissue types. As suggested by Cherel et al. (2010), we used
1.7‰ as the enrichment factor between prey muscle and
seabird and marine mammal blood (Hobson et  al. 1996;
Cherel et al. 2005). Hence, we used the following equation
to estimate TP for seabirds and fur seals:
TPconsumer = 𝛾baseline + 1 + 𝛿 15 Nconsumer −1.7−𝛿 15 Nbaseline ∕Δ15 N
( ) [( ) ]

Results

Stable isotope results (without modelling)

In total, we measured δ13C and δ15N values for 831 sam-

ples from 13 taxa within the Peruvian marine food web
that were collected between 2008 and 2011 (Fig.  1;
Table 1). Both δ13C and δ15N values showed a high iso-
topic variability between and within taxa (Fig.  2). The
mean δ15N values ranged from 7.6‰ (copepods) to
18.3‰ (fur seal) (Fig. 2). The highest δ15N values were
found for the fur seal, seabirds and jack mackerel. Cope-
pods, euphausiids and myctophids had the lowest δ15N
values (Table  1; Fig.  2). Mean δ13C values ranged from
Fig. 3  δ13C values vs. sampling distance to the coast for organisms
−20.3‰ for copepods to −14.7‰ for the Peruvian booby collected in the NHCS. Values are ± SD
(Table  1; Fig.  2). δ13C values >-17‰ were observed in
samples collected <100  km from the coast (e.g., sea-
birds, squat lobster, Fig. 3). On the other hand, δ13C val-
ues were <−18‰ (e.g., mesopelagic fishes, mackerel) at

13
Mar Biol (2017) 164:86 Page 7 of 15  86
a distance >200  km from the coast. Seabirds and squat
lobsters had the highest δ13C values (−15, −14.7 and
−15.2‰) associated with the lowest variability (0.1 to
0.4‰), while copepods, euphausiids and mesopelagic
fish had the lowest δ13C values (−20.3, −18.1, −19.0
and −18.5‰, Table 1) with relatively high inter-individ-
ual variability (0.9–1.3‰). Fur seals also showed com-
paratively low δ13C values (−16.9‰) when taking into
account the distance to the coast of the sampling site
(0 km since they were sampled in a peninsula).
The relationships between δ13C and δ15N values vs. body
length and latitude were plotted for each species (Figs.  4,
5). A size effect was detected for some groups only. δ15N
values significantly (p < 0.01) increased linearly with body
length for hake (a 2.5‰ range) and jumbo squid (Fig.  3,
~5.0‰). Noting the unbalanced sampling scheme, δ15N
values of euphausiids, squat lobster, anchoveta and fur seal
showed no obvious relationship with body length, while
jack mackerel exhibited a decreasing linear trend. Strong
latitudinal variations were then depicted in the δ15N values
of jumbo squids and anchoveta (Fig. 5). δ15N values stead-
ily decreased from 18.0°S to ~7.5°S and then stabilised.
Fig. 4  Body length -based variability of δ15N values. Black and white dots illustrate the different latitude groups (north vs. south of 7.5°S)
Species only sampled north of 7.5° (hake, myctophids and
euphausiids) did not show any latitudinal trend.
LME models
The LME models predicted δ15N values taking into account
both the variability in baseline δ15N values (with latitude)
and the body size effect. Two models were fitted on the
data (north and south of 7.5°S). Both models treated the
species effect as random but differed in their structure. The
best model for the northern area had a fixed effect on both
body size and latitude with a random species effect on the
intercept, while the best model for the southern area had a
fixed effect for body size and a random species effect for
the latitude slope (Tables S1, S2).
Model results for fixed body size (i.e., according to
the size range of the species, Fig.  6) illustrate the differ-
ent latitudinal effects on δ15N values. South of 7.5°, δ15N
values strongly decrease towards the north. The trends are
species dependent (random latitudinal effect in the model)
with higher slopes for anchoveta and jack mackerel than for
jumbo squid or squat lobster. North of 7.5°S the slopes are
13
 86   Page 8 of 15 Mar Biol (2017) 164:86

Fig. 5  Latitudinal variability of δ15N values. The vertical line represents the 7.5°S threshold

similar for all species (fixed latitudinal effect) and much

less pronounced than further south. Comparing predicted
δ15N values of consumers between the northern and south-
ern regions highlighted different patterns among species
(Table 2). At 7.0°S, the squat lobster had the highest δ15N
value (11.8‰), when compared to hake (11.5‰), mackerel
(11.4‰), jumbo squid (11.1‰) and anchoveta (10.9‰).
At 11.7°S, top predators that were not sampled in the north
showed the highest δ15N values (fur seal: 16.0‰, jack
mackerel: 15.1‰, Guanay cormorant: 15.0‰, Peruvian
booby: 14.6‰). They were followed in a decreasing δ15N
order by the jumbo squid (14.3‰), squat lobster (13.6‰),
anchoveta (13.5‰), the mesopelagic fish Vinciguerria
(12.6‰), mackerel (12.4‰) and copepod (9.5‰).

Trophic position

Mean TPs were estimated with predicted δ15N values

Fig. 6  Predicted δ15N values from the two LME models: north and for fixed sizes at two latitudes, 11.7 and 7.0°S (Table 2;
south of 7.5°S. For each species the latitudinal range of prediction
covers the one where individuals were sampled. No predictions were Fig. 7). The trends are logically identical to those previ-
made when only one sampling location was available (dots) ously described using predicted δ15N values (see above)

13
Mar Biol (2017) 164:86 Page 9 of 15  86
Fig. 7  Predicted trophic positions (TP) at 11.7°S (Vinciguerria, mackerel, squat lobster, anchoveta, jumbo squid, jack mackerel, peruvian booby,
guanay cormorant, fur seal) and 7.0°S (euphausiids, myctophids, Vinciguerria, anchoveta, jumbo squid, mackerel, hake and squat lobster)
due to the direct linear scaling of estimated TP with δ15N.
At 7.0°S, estimated TPs ranged from 2.8 for euphausi-
ids to 3.7 for squat lobster. At 11.7°S, TPs ranged from
3.3 for mackerel to 4.9 for fur seal. The TP rank between
common species was different at 11.7 and 7.0°S. The
squat lobster had a higher TP (3.7) than jumbo squid (3.5)
at 7.0°S, but its TP was lower (3.7 vs. 3.9) at 11.7°S.
Discussion
Using stable isotope analyses, we focused on a simpli-
fied but representative (13 components) food web in the
northern Humboldt Current system (NHCS). The δ15N
baseline is strongly impacted by variability in the OMZ
intensity along the Peruvian coast (Mollier-Vogel et  al.
2012). Hence, a modelling approach was developed to
account for such external variability to estimate trophic
positions of key pelagic organisms. In spite of limitations
due to the unbalanced nature of our data set and assump-
tions used to estimate TP, some patterns emerged, thus
providing new insights on trophic relationships within
this highly productive ecosystem. In particular, we con-
firmed the high TP of anchoveta, and bring attention to
the potentially important role of the abundant squat lob-
ster, a previously understudied pelagic species within the
NHCS.
Pattern of variability in δ13C
Our study revealed a general trend of increasing δ13C and
δ15N values from copepods to larger organisms (Fig.  2).
This classic pattern shows the well-known 13C and 15N
enrichments up the trophic food web (e.g. Stowasser et al.
2012). An overall decreasing trend in organism δ13C values
was also observed with lower δ13C values when increasing
sampling distances from the shore (Fig.  3). Such inshore/
offshore patterns are expected in many ecosystems, includ-
ing in upwelling systems (Sydeman et al. 1997; Miller et al.
2008). The species δ13C values should decrease following
the order coastal > neritic > oceanic species because δ13C
values of particulate organic matter decreases from inshore
to offshore waters with the decrease of productivity (Hill
et  al. 2006). A decreasing cross-shore trend in productiv-
ity in the NHCS has also been estimated from Chl-a con-
centration (Demarcq 2009). The δ13C values can then be
interpreted in terms of inshore or offshore foraging habi-
tat. The highest δ13C values were observed for seabirds
and squat lobsters, which would indicate a narrower costal
foraging area compared to mesopelagic fish and euphausi-
ids which would tend to forage offshore. Tagging studies
on birds indeed showed that these two species were feeding
in the first tens of kms from the colony, close to the coast
(Weimerskirch et  al. 2010). Anchoveta and squat lobster
overlap in their δ13C values, with anchoveta exhibiting a
much larger range of δ13C (−20.6 to −13.8‰ vs. −16.0 to
13
 86   Page 10 of 15
−14.3‰) suggesting that the former feeds both inshore and
offshore, and has a larger foraging range than squat lobsters
which are more restricted to inshore pelagic waters. Fur
seals, while sampled at the coast, had intermediate δ13C
values, which can be explained by the fact that this species
forage offshore at ~50–100  km from the coast (Y. Trem-
blay, unpublished data). Compared to other species, iso-
topic values of seabirds and fur seals had a narrower range
(in both C and N isotopes), suggesting a localized and spe-
cialized diet (central place foragers). Jumbo squids, mack-
erel and anchoveta showed large variance in their isotopic
signatures (Fig.  2), even when considering only one sam-
pling site, which indicates wider isotopic niches and inter-
individual differences in their foraging ecology (different
habitats and/or food items, size-based feeding preferences).
Pattern of variability in δ15N
Along with the increase in trophic level (Fig. 2), the clear-
est pattern in δ15N values relates to baseline changes with
latitude (Fig.  5). An increasing trend of δ15N values from
north to south with a shift around 7.5°S was observed.
This trend had already been reported in previous studies
(Lorrain et  al. 2011; Argüelles et  al. 2012; Ruiz-Cooley
and Gerrodette 2012) and can be related to changes in the
δ15N values of the baseline modulated by the OMZ inten-
sity along the Peruvian coast (Bertrand et  al. 2010; Mol-
lier-Vogel et al. 2012). Indeed, in OMZ, strong denitrifica-
tion and anammox are known to occur, and recent studies
showed that anammox is the main nitrogen loss process in
the Peruvian OMZ (Lam et al. 2009; Kalvelage et al. 2013).
Denitrification in anoxic water has a large isotope effect of
~-25‰ (Voss et al. 2001). To date, little is known about the
isotope fractionation of anammox in the water column, but
it is generally assumed that it has similar isotope fractiona-
tion than denitrification (Naqvi et al. 2006), producing ­NO3
and organic matter strongly enriched in 15N (up to 20‰,
Voss et  al. 2001). The intensification of oxygen deficient
conditions in Peru south of ~7.5°S (Bertrand et  al. 2010)
would then contribute to a latitudinal gradient in δ15N base-
line, with highest δ15N values in the south. This north to
south δ15N gradient has also been observed in sediments
along the Peruvian margin (Mollier-Vogel et  al. 2012). In
the north (1°N to 7°S), sediment δ15N values are relatively
low and uniform, ranging only between 4 to 5‰, while
δ15N values increase southward from 4.5 to 13.0‰. These
changes in δ15N baseline are then transferred through the
food web, as observed in the δ15N values of pelagic con-
sumers (Fig. 7).
Another factor impacting δ15N values was body size.
This size effect was most evident for the jumbo squid and
hake, for which we sampled a large range of body size.
The jumbo squid is known to increase its TP with size
13
Mar Biol (2017) 164:86
(Argüelles et  al. 2012; Ruiz-Cooley and Gerrodette 2012;
Alegre et al. 2014) even if at individual level, large D. gigas
can shift toward a diet dominated by euphausiids (Lor-
rain et  al. 2011). TP of hake increases with size because
cannibalism is more frequent in larger individuals which,
consequently, consume less euphausiids (Tam et al. 2006).
The pattern is not as clear for anchoveta and opposite in
Jack mackerel, which showed a decreasing δ15N pattern
with size. These null or negative trends are most probably
due to interaction with latitude that was further corrected
in the LME models. Anchoveta, indeed, have been shown
to increase their TP with size due to an increased propor-
tion of euphausiids and decreased proportion of copepods
in their diet as they grow (Espinoza and Bertrand 2014).
Similarly, larger jack mackerel increase their predation on
fish with size, thus consuming less copepods (Alegre et al.
2015).
Predicted δ15N values and trophic positions
The impact of the OMZ on the δ15N baseline and the cor-
responding shift at ~7.5°S led us to construct two separate
LME models, south and north of 7.5°S. The unbalanced
sampling scheme and the actual species distribution (e.g.
hake is mostly present in the north) explain why each
model includes different species. The lack of latitudinal
and body size coverage for several species also weakens the
predictive power of the constructed models. Furthermore,
in the southern region, we observe different slopes for some
species (Fig. 6), indicating that these species might not be
in isotopic equilibrium with their diet and that they might
come from another foraging location. TP estimates in the
south might, therefore, not be as representative as in the
northern region. Finally, as outlined in methods, several
assumptions were made for consistency and comparability
with other similar studies, i.e. TP were estimated using a
fixed discrimination factor of 3.4‰ (Hückstädt et al. 2007;
Miller et al. 2010) and a TP of 2.5 for copepods. The result-
ing TP estimates should necessarily be taken with cautious.
For example, using a TP for copepods of 2 instead of 2.5
would lower the TP estimates by 0.4 TP, only. We have also
estimated TP with the scaled framework recently proposed
by Hussey et  al. (2014), which uses narrowing discrimi-
nation factors dependant on the species and their diet and
found very similar results with differences of TP estimates
of maximum 0.1 and no change in the relative position of
species. Despite these shortcomings, we are confident in
the relative positions of species and on the emerging pat-
terns (Fig. 7).
First, euphausiids, which are dominated by Euphau-
sia mucronata in the NHCS (Ayón et  al. 2008b), are at a
higher trophic level than copepods (predicted TP: 2.8).
These results differ from those of Hückstädt et  al. (2007)
Mar Biol (2017) 164:86 Page 11 of 15  86

who proposed a TP of 2.0 for E. mucronata off Chile. In
the California Current system, Sydeman et al. (1997) esti-
mated TP of Euphausia pacifica to be 2.5, while Miller
et al. (2010) estimated TPs of Euphausia pacifica and Thy-
sanoessa spinifera to be 2.1 and 2.3, respectively. The high
TP found in the NHCS is not unrealistic as some krill spe-
cies can have a TP ≥3, for instance Euphausia frigida (3.0)
and Euphausia tricantha (3.3) in Antarctic waters (Stowas-
ser et al. 2012).
Second, estimated TP for anchoveta (3.4–3.7) are in
accordance with the results of Espinoza and Bertrand
(2008), which showed that zooplankton was the most
important dietary component of anchoveta, with euphausi-
ids contributing 67.5% of dietary carbon followed by cope-
pods (26.3%). TP estimates for various Engraulis spp.
around the world (Table  3) vary between 2 and 4, most
ranging between 3.0 and 3.6. Our TP estimates for ancho-
veta are thus in the higher range of TP estimations but simi-
lar to Hückstädt et al. (2007) who estimated TP of E. rin-
gens to 3.6. Such a high TP for E. ringens when compared
with other Engraulis spp. is not surprising, since E. ringens
forage on larger prey than anchovies from other EBUSs
(Espinoza et  al. 2009). Mesopelagic fishes (Vinciguerria
lucetia and myctophids) emerge as secondary consumers
with a predicted TP between 2.9 and 3.4. These estimates
are comparable to what has been observed in other Eastern
Boundary Upwelling Systems (EBUS): 3.4 in the Califor-
nia Current system (Choy et al. 2012) and 2.7 in the north-
ern Benguela Current system (Iitembu et al. 2012).
Patterns for organisms with TP above that of ancho-
veta are less clear. The squat lobster showed the highest
TP (3.8) in the northern region, i.e. above the hake (3.7)
or the jumbo squid (3.5). We do not explain this high value
compared to these two species and we cannot reject that
this could be due to a different discrimination factor for
this species or the use of pelagic copepods for the isotopic
baseline if squat lobsters forage in some cases in coastal or
benthic ecosystems. In the southern region the estimated
TP of squat lobster was still high (3.6), but lower than a
jumbo squid of 40 cm (3.8) (although this small difference
could be the result of our unbalanced database). Noting
that anchoveta and squat lobster share a similar ecologi-
cal niche, Gutiérrez et  al. (2008) stated that “a potential
negative competition and predation exists between these
species”, and posited that squat lobster could forage on
fish eggs and larvae, and be a predator of first stages of

Table 3  Trophic position estimates of some Engraulis spp. around the world

Species Sampling areas Methods Stage TP References

Engraulis anchoita Argentinian coast Volumetric Juveniles and adults 2–4 Angelescu (1982)
Engraulis encrasicolus Catalan Sea—Gulf of Lions Stomach contents Larvae 3.1–3.7 Tudela et al. (2002) from
http://www.fishbase.org
West coast of South Africa Carbon contents Juveniles and adults 3.3 Armstrong et al. (1991)
calculated here
Atlantic coast of the Iberian δ15N Juveniles and adults 3.4 Bode et al. (2007)
Peninsula
Gulf of Lions (Mediterra- δ15N Adults 2.4–2.9 Costalago et al. (2012)
nean Sea)
Gulf of Lions (Mediterra- δ15N Juveniles 2.3–3.1 Costalago et al. (2012)
nean Sea)
Gulf of Lions (Mediterra- δ15N Late-larvae 2.4 Costalago et al. (2012)
nean Sea)
Engraulis japonicus Southern Japan δ15N Adults 3.3 Takai et al. (2007)
Southern Japan δ15N Larvae and juveniles 3.0 Takai et al. (2007)
Engraulis mordax California Current Stomach contents Juveniles and adults 3.0 Kucas (1986) from http://
www.fishbase.org
California Current δ15N Adults 3.1 Miller et al. (2010)
Engraulis ringens Central Chile % mass and Ecopath esti- Adults 2.1 Neira and Arancibia (2004)
mation
Northern Chile % mass and Ecopath esti- nd 2.9 Medina et al. (2007)
mation
Central Chile δ15N nd 3.6 Hückstädt et al. (2007)
Peruvian coast Carbon content Juveniles and adults 3.5 Espinoza and Bertrand
(2008)a
Peruvian coast δ15N Adults (14 cm) 3.4–3.5 This study
a
 Calculated from the diet results of Espinoza and Bertrand (2008) following the method from Christensen and Pauly (1992)

13
 86   Page 12 of 15
harvested fish species (including anchoveta). While the
similar TP observed here for squat lobster and anchoveta
could imply that the two species compete, their different
δ13C values suggest that they do not exactly share the same
habitat, with anchoveta having a larger and more offshore
foraging range. This is indeed what Gutiérrez et al. (2008)
observed through acoustic survey performed between 1998
and 2006 along the Peruvian coast, with the squat lob-
ster restricted to a more coastal region when compared
to anchoveta, which could reduce direct competition for
resources. In Chile, benthic Pleuroncodes monodon for-
ages on amphipods, zoeas, crustacean eggs, diatoms, fora-
minifers, bacteria, organic wastes and fish scales (Gallardo
et  al. 1980), while in the California Current, pelagic P.
planipes feeds on protists, zooplankton (mainly copepods,
euphausiids and chaetognaths) and large diatoms (Long-
hurst et al. 1967). Specific diet studies should thus be per-
formed on squat lobster to further understand its role in the
NHCS food web and to elucidate to what extent this role is
impacted by the benthic vs. pelagic lifestyle shown by dif-
ferent species within this taxon.
The estimated TP for jumbo squid ranged from 3.5
(north) to 3.9 (south) for specimens of 40  cm ML. Such
results follow those of Hückstädt et  al. (2007) who esti-
mated jumbo squid TP to 3.8 in Chile, and of Miller et al.
(2013) who found a large proportion of macrozooplankton,
ichthyoplankton and small fish in the diet of this species in
the northern California Current. However, such estimates
are rather low considering dietary studies in the NHCS
showing that Dosidicus gigas mainly forage on cephalo-
pods and fish (Alegre et al. 2014). A similar phenomenon
occurs for hake (Merluccius gayi peruanus, estimated TP:
3.6), which mainly forage on fish and squids (Tam et  al.
2006), with crustaceans only amounting to ~15% of the
fish diet. However, our estimates match those for other hake
species, e.g. Merlucius gayi gayi in Chile (TP: 3.6, Hück-
städt et  al. 2007), Merlucius productus in California (TP:
3.3, Miller et  al. 2010), and Merlucius capensis in South
Africa (TP: 3.0-3.6, Iitembu et al. 2012).
The mackerel Scomber japonicus showed a lower
trophic level (3.3–3.6) than the jack mackerel Trachu-
rus murphyi (4.2). Although Alegre et  al. (2015) showed
that mackerel consume more fish than jack mackerel this
result is logical since TP have been predicted for smaller
mackerel (200 mm) than jack mackerel (250 mm). Our esti-
mates for S. japonicus are similar with those in California:
3.4 (Miller et al. 2010) and, to a lesser extent in the Bay of
Bicay: 3.7 (Chouvelon et al. 2012). In the case of the jack
mackerel our estimated TP is higher than those from Hück-
städt et al. (2007) in Chile (3.4) and Miller et al. (2010) in
California (T. symmetricus, TP: 3.6).
Finally and as expected, the air-breathing top predators
had the highest estimated TP: 4.5 for the Peruvian booby,
13
Mar Biol (2017) 164:86
4.6 for the Guanay cormorant that feed almost exclusively
on anchoveta (Zavalaga and Paredes 1999), and 4.9 for the
fur seal, which is known to forage on small epi- or meso-
pelagic fish, with a possible preference for adult anchoveta
(Majluf 1989). These results match those already reported
in the literature: Sydeman et al. (1997) estimated TP of cor-
morants Phalacrocorax pelagicus and Phalacrocorax peni-
cillatus to 4.3 and 4.5, respectively, Hückstädt et al. (2007)
measured a TP of 4.6 for the sea lion Octavia flavescens,
and Cherel et al. (2010) reported a TP of 4.8 for the Antarc-
tic fur seal Arctocephalus gazella.
Conclusion
This study provided TP estimates for 13 important taxo-
nomic groups in the NHCS from zooplankton to top preda-
tors. The objective of this work was not to propose a defini-
tive answer to the “moderate primary productivity, high
fish productivity” paradox, but to provide supplementary
data to assist in its appraisal. Indeed, with an estimated
TP ranging between 3.4 and 3.7 for anchoveta, our results
further challenge the Ryther’s (1969) short food chain
hypothesis, following Espinoza and Bertrand (2008, 2014)
that demonstrated a dominance of zooplankton in ancho-
veta diet. The long food chain we showed here could be
explained by the very efficient bottom-up transfer described
by Bertrand et al. (2014) for the NHCS, in which prey are
concentrated within a thin surface layer and more specifi-
cally within “pelagic oases” created by fine scale physical
structures that would facilitate the energetic transfer. We
also discuss the potential importance of an often neglected
ecosystem component, the squat lobster. Further studies on
this species, focusing on fatty acids or compound specific
isotope analysis of specific fatty acids, are necessary as we
were not able to infer its role in the diet of air-breathing top
predators neither its relation with anchoveta. Amino acid
compound specific stable isotope analysis is now required
to further validate the TP estimates provided in this study.
Finally, given the differences between the past and current
descriptions of the trophic ecology of important species in
the NHCS, in particular the anchoveta, our results are key
to revisiting ecosystem models for this system.
Acknowledgements  This work is a contribution to the cooperative
agreement between the Instituto del Mar del Peru (IMARPE), the
Institut de Recherche pour le Developpement (IRD), and of the LMI
DISCOH. This publication was made possible through support pro-
vided by the ANR TOPINEME. We would like to thank G. Guillou
from the LIENSs laboratory for stable isotope analysis, and the two
anonymous reviewers for their constructive comments on the manu-
script. PE was financially supported by the BEST Grant from IRD and
managed by Campus France.
Mar Biol (2017) 164:86 Page 13 of 15  86
Compliance with ethical standards  tropical Pacific. PLoS ONE 6(12):e29558. doi:10.1371/jour-
This study was funded by IRD, IMARPE and ANR TOPINEME. None
of the coauthors have ethical issues arising from conflicts of interest.
All applicable international, national, and/or institutional guidelines
for the care and use of animals were followed.
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