Received: 22 May 2018 | Revised: 3 August 2018 | Accepted: 5 October 2018

DOI: 10.1111/fog.12419

ORIGINAL ARTICLE

Anchovy distribution off Peru in relation to abiotic

parameters: A 32‐year time series from 1985 to 2017

Ramiro Castillo1,2 | Luciano Dalla Rosa3 | Walter García Diaz2 | Lauro Madureira1 |
Mariano Gutierrez4 | Luís Vásquez2 | Rolf Koppelmann5

1
Hydroacoustics Lab, Biological
Oceanography, Federal University of Rio Abstract
Grande (FURG), Rio Grande do Sul, Brazil Oceanographic and hydroacoustic data were obtained by the Instituto del Mar del
2
Instituto del Mar del Peru (IMARPE),
Peru (IMARPE) during 72 cruises off the Peruvian coast between 1985 and 2017 to
Callao, Peru
3
Oceanography Institute, Federal University determine the ranges of the abiotic parameters influencing the anchovy (anchoveta)
of Rio Grande (FURG), Rio Grande do Sul, distribution and to observe the effect of the 1997–1998 El Niño event. The hydroa-
Brazil
4
coustic data show a high seasonal variability in anchoveta distribution related to dif-
Faculty of Oceanography, Fisheries, Food
Science and Aquaculture, Federal University ferences of environmental parameters as well as changes in distribution after the
Federico Villarreal, Miraflores, Lima, Peru
very strong El Niño event in 1997–1998. Geostatistic variograms were used to
5
Center for Earth System Research and
Sustainability (CEN), Institute for Marine
describe the seasonal variability and generalized additive models (GAMs) with a
Ecosystem and Fisheries Science (IMF), Tweedie distribution were applied to study the relationships between anchoveta
University of Hamburg, Hamburg, Germany
and oceanographic parameters. The dependent variable was the value for anchoveta
Correspondence obtained from echosounder (nautical area scattering coefficient [NASC] of ancho-
Ramiro Castillo, Hydroacoustics Lab,
Biological Oceanography, Federal University
veta) and the tested covariates were temperature, salinity, and dissolved oxygen at
of Rio Grande (FURG), Rio Grande do Sul, the sea surface; distance to the coast; year, latitude–longitude; and Oceanic Niño
Brazil.
Email: ramirocasti@gmail.com
Index 1 + 2. The results show a high variability of anchoveta with seasonal differ-
ences in its distribution. Preferred abiotic conditions (temperature, salinity, oxygen)
of anchoveta were 17.6–23.7°C, 32.30–35.14, and 5.9–8.7 ml/L in summer and
14.5–18.8°C, 34.81–35.12, and 5.2–6.3 ml/L in winter. The values in autumn and
spring were intermediate and are considered as in transition. The anchoveta were
detected at higher values after the 1997–1998 El Niño event, probably influenced
by reduced standing stocks of congener fish species and by the Pacific decadal
oscillation (PDO) or by a changes in climate.

KEYWORDS
anchoveta, anchovy, El Niño, generalized additive model, hydroacoustics, Peru, Tweedie
distribution

1 | INTRODUCTION climate variability. Climate variability affects fish behavior (Checkley,

The Northern Humboldt Current System (NHCS) is influenced by an
intense regional climate variability at different spatiotemporal scales
(Chavez, Bertrand, Guevara‐Carrasco, Soler, & Csirke, 2008). Due to
nonlinear relationships between oceanographic and biological param-
eters, it is difficult to understand how marine ecosystems respond to
Asch, & Rykaczewski, 2017; Lehodey et al., 2006; Swartzman, Ber-
trand, Gutiérrez, Bertrand, & Vasquez, 2008; Tinvergen, 1963) and
the Peruvian anchovy or anchoveta (Engraulis ringens) in particular.
The response of anchoveta populations to climate variability can be
investigated by observing changes in their habitat. Bertrand et al.
(2008) and Gutiérrez, Castillo, Segura, Peraltilla, and Flores (2012)

Fisheries Oceanography. 2018;1–13. wileyonlinelibrary.com/journal/fog © 2018 John Wiley & Sons Ltd | 1
2 | CASTILLO ET AL.

detected that physical and chemical variability of the oceanographic proxies for the distribution patterns to improve the explained
system influences the abundance of anchoveta. The variability of dis- deviance and better predict anchoveta distributions.
tinct water masses, particularly the cold coastal waters (CCW), influ-
ences the anchoveta density despite the total stock of the
2 | MATERIALS AND METHODS
population (Swartzman et al., 2008). In summer, anchoveta are usu-
ally located in large schools near the coast; in winter, the anchoveta
2.1 | Data collection
move away from the coast and schools are more dispersed (Sim-
monds et al., 2009), less dense, and linked to nutrient‐rich CCW Acoustic and oceanographic data were collected on 72 surveys car-
(Morón, 2000). Natural disturbances in the environment like El Niño ried out by the Instituto del Mar del Peru (IMARPE) along the Peru-
events affect the distribution and abundance of anchoveta. During vian coast (03°23′S–18°21′S) between 1985 and 2017. The data
an El Niño, when the upwelling at the coast is reduced or collapsed, were collected by applying a systematic sampling strategy on tran-
anchoveta migrate southward in search for colder waters, causing sects perpendicular to the coast (Figure 1, Table 1) usually separated
changes in size structure and reproduction (Ñiquen & Bouchon, by ca. 14–15 nm (Castillo et al., 2011; Simmonds & MacLennan,
2004). 2005). Samples were taken in spring (October, November, Decem-
Different models such as generalized linear models (GLMs), gen- ber), summer (January, February, March), autumn (April, May, June),
eralized linear mixed models (GLMMs), and generalized additive and winter (July, August, September).
models (GAMs) were applied to explain effects of changing environ-
mental parameters on fishes (Francis, Morrison, Leathwick, Walsh, &
2.2 | Acoustic and oceanographic data
Middleton, 2005; Planque, Bellier, & Lazure, 2007; Riou, Le Pape, &
Rogers, 2001). The disadvantage of the first two models is that they Acoustic data were collected using different SIMRAD scientific echo-
only detect linear relationships between the parameters and the sounders: from 1985–1991 EK, EKS, and EK400; from 1992–1995
fishes. A GAM, however, is a nonparametric regression technique EK38; from 1996–1997 EY500; from 1997–2007 EK500 with 38
not restricted to linear relations (Hastie & Tibshirani, 1990) and is and 120 kHz; from 2007–2017 EK60, the 200 kHz frequency was
flexible in terms of the statistical distribution of the data (Swartzman, added in 2008 and 12 and 70 kHz were added in 2014. Particularly,
Silverman, & Williamson, 1995). Several studies on fish distribution the anchoveta data were obtained at a frequency of 120 kHz. Dur-
use GAMs and acoustic and oceanographic data, for example, for ing each survey, the echo integration acoustic method (Simmonds &
herring (Clupea harengus) in the Atlantic (Bailey, Maravelias, & Sim- MacLennan, 2005) was applied, that is, transmitting sound at high
monds, 1998; Maravelias, 1997; Maravelias & Reid, 1995; Mar- frequencies into the water column and quantifying and interpreting
avelias, Reid, & Swartzman, 2000), for Alaska pollock (Theragra reflections of acoustic energy from objects or organisms. The ratio
chalcogramma) in the Bering sea (Swartzman, Stuetzle, Kulman, &
Powojowski, 1994), for pelagic fish and krill (Euphausia superba) in
84ºW 82ºW 80ºW 78ºW 76ºW 74ºW 72ºW 70ºW
the sea of Japan (Murase, Nagashima, Yonezaki, Matsukura, & Kita-
kado, 2009), for sardines (Sardinops sagax) and other pelagic fishes in
4°S Pta. Sal 4ºS
the California Current (Zwolinski et al., 2012), for anchoveta (Engrau- Talara
Paita
lis encrasicolus) and other pelagic species in the Aegean Sea in the
6°S Pta. La Negra 6ºS
eastern Mediterranean (Giannoulaki et al., 2008), and for cod (Gadus
Pimentel
morhua) and haddock (Melanogrammus aeglefinus) in the North Sea
Malabrigo
(Hedger et al., 2004). A Tweedie dispersion model can be applied in 8°S Salaverry 8ºS

GAMs if zero values are present in the acoustic samples of ancho- Chimbote
Casma
veta (Poisson‐gamma distribution). Other applications in GLMs and 10°S Huarmey 10ºS
Supe
GLMMs provide more efficient and realistic estimations in catch and Huacho
Chancay
effort data (Candy, 2004). 12°S Callao 12ºS
Pucusana
We studied the influence of oceanographic parameters, mainly P Cerro Azul
Pisco
80

temperature, salinity, and oxygen, on the distribution of anchovy in 14°S Bahia Independencia 14ºS
different seasons and investigated environmental conditions before
San Juan Marcona
and after the very strong El Niño event in 1997/1998. A decrease in 16°S Atico 16ºS
biomass of the main cohabitant fish species of anchoveta such as Mollendo
Ilo
sardine, horse mackerel, and mackerel was detected after the 1997– 18°S Sama 18ºS
1998 El Niño event (Gutiérrez et al., 2012). We hypothesize that
84°W 82°W 80°W 78°W 76°W 74°W 72°W 70°W
seasonally changing abiotic parameters such as temperature, salinity,
and dissolved oxygen cause a change in abundance and distribution F I G U R E 1 A typical hydroacoustic sampling scheme during one
of anchoveta. In our models, we used these abiotic parameters as cruise with systematic transects separated by 14–15 nm is presented
CASTILLO ET AL.
T A B L E 1 Acoustics samples analyzed during each season
Number of Acoustics
Season (months) cruises samples
Summer (January, February, 26 173,562
March)
Autumn (April, May, June) 8 28,583
Winter (July, August, September) 21 121,184
Spring (October, November, 17 101,932
December)
Total 72 425,261
between transmitted and reflected energy is the nautical area scat-
tering coefficient (NASC) expressed in m2/nm2 and was obtained
down to 500 m depth. Elementary distance sampling units (EDSUs)
were calculated for one nautical miles from 1985 to 1993 and for
two nautical mile between 1994 and 2017 according to FAO recom-
mendations (Gutiérrez et al., 2012).
Concentrations and characteristics of echotraces were related to
fish species caught in pelagic trawls for all NASC values and each
ESDU between 1983 and 1999. Since 2000, the ECHOVIEW software
was used to identify echotraces of specific species (Castillo et al.,
2011), which facilitated the identification of the species. The values
obtained for the anchoveta in each ESDU (NASC anch) were used in
this analysis.
Oceanographic data (temperature, salinity, oxygen, depth) were
measured at each hydrographic station with thermometers, conduc-
tivity–temperature–depth sensors (CTDs), Niskin bottles, and/or CTD
rosettes. Generally, these stations were located on nine transects
perpendicular to the coast off Paita, Punta La Negra, Chicama, Chim-
bote, Callao, Pisco, San Juan de Marcona, Ático, and Ilo. These tran-
sects are separated by 20 nm in average and were carried out in
addition to the oceanographic measurements at the trawling sta-
tions. Salinity was analyzed with a salinometer, and oxygen was
measured using the Winkler method modified by Carrit and Carpen-
ter (1966). Temperature (°C), salinity, and dissolved oxygen at the
sea surface (ml/L) were spatially interpolated for acoustic samples
using the slice command of the SURFER software for each ESDU. In
total, 425,261 acoustic samples with oceanographic data were ana-
lyzed (Figure 1, Table 1).
2.3 | Other variables collected
Further information obtained for each EDSU was bottom depth (m)
from echosounder, distance to coast (nm), cruise period (month, sea-
son and year), position data (latitude and longitude), and the Oceanic
Niño Index (ONI) for the region 1 + 2 (0–10°S, 90–80°W). The
Oceanic Niño Index is NOAA's (National Oceanic and Atmospheric
Administration) primary indicator for monitoring El Niño and La Niña,
which are opposite phases of the climate pattern called the El Niño‐
Southern Oscillation, or “ENSO” for short. NOAA considers El Niño
conditions to be present when the Oceanic Niño Index is +0.5 or
higher, indicating that the east‐central tropical Pacific is significantly
warmer than usual. La Niña conditions exist when the Oceanic Niño
| 3
Index is −0.5 or lower, indicating that the region is cooler than usual.
The Niño 1 + 2 region is the smallest and eastern‐most Niño region
and corresponds with the region of coastal South America where El
Niño was first recognized by the local populations. This index can
also be used as a proxy for the distribution of species (McClatchie,
2014); it was obtained from the monthly average for each cruise
period on the NOAA website: http://www.cpc.ncep.noaa.gov/data/
indices/ersst3b.nino.mth.81-10.ascii.
2.4 | Time variability
Due to the high variability in data, the fluctuations of anchoveta
NASC values for each cruise were visualized using a boxplot with
logarithmic transformation (NASC) + 1. Spatial structure of the
NASC values was realized by geostatistic variograms using a spheri-
cal model. This model assumes an almost linear growth and that cer-
tain distances finite of the origin reach a stabilization (sill; Deutsch &
Journel, 1998). The analyses were performed in the EVA (VAriance
Estimation) software described by Petitgas and Lafont (1997), and
variogram values were exported to a spreadsheet using the following
parameters (Bez & Fernandes, 2002):
Sampling: Scheme B, Method Intrinsic 2D
Variable: s1<=z<=s2
Structure: Polygons make, show, study area definition with inte-
rior points
Model: Spherical, Estimator using squares differences; parameters:
nb lag 60, lag 1, tolerance 0, 5, 2D, angle 60.
The least squares model was used to fit the variogram model to
the experimental data as described by Cressie (1993). The standard-
ized variograms for all cruises were separated by station.
2.5 | Data exploration
An exploratory analysis was performed on the response variable
(i.e., NASC values) and the explanatory variables (i.e., temperature,
salinity, and dissolved oxygen at the sea surface, distance to the
coast, year, latitude–longitude, and the Oceanic Niño Index 1 + 2)
to identify the spatial autocorrelations of the response variable, sea-
sonal differences (boxplots), and collinearity correlation of the
explanatory variables by the spearman method (pairplots; Zuur,
2012).
2.6 | Statistical modeling
Generalized additive models were used to study the relationship
between anchoveta NASC values and explanatory variables. The
explanatory variables were sea surface temperature (SST in °C), sea
surface salinity (SSS), and sea surface oxygen (SSO in ml/L). In addi-
tion, the following variables were considered as they could affect
the distribution of anchoveta, especially in the north: depth (bottom
in meters), distance to the coast (dc in nautical miles), season, month,
4 |
year, position (latitude in °S and longitude in °W), and the Oceanic
Niño Index 1 + 2 (ONI).
The applied model is as follows:
YðanchÞ ¼ β þ f1ðsstÞ þ f2ðsssÞ þ f3ðssoÞ þ f4ðbottomÞ þ f5ðdcÞ
þ f6ðseasonÞ þ f7ðmonthÞ þ f8ðyearÞ þ f9ðpositionÞ
þ f10ðONIÞ þ ɛ
where Y(anch) is a predictor variable, β is an intercept, fi(Xi)
represents the polynomial function that tries to explain the variation
of the dependent variable Y with the predictor variable Xi, and ε is
the error.
We used the cubic spline regression (cr) for smooth functions
which consists of a set of cubic polynomials with first and second
continuous derivatives at the nodes. This function has the advantage
of being computationally simple with directly interpretable parame-
ters (Wood, 2006). The year variable was considered as discrete. In
case of position, longitudes and latitudes were attenuated by the
interaction of tensor products of thin plate regression splines (tp),
which considers isotropic as a reasonable assumption for spatial
dependence (Wood, 2011). The smoothing parameter determines
the smoothness of the estimate and was determined by the general-
ized cross validation (GCV) criterion (Marra & Wood, 2011).
Data from this study were influenced by a high proportion of
zeros (72.6%), that is, data with no presence of anchoveta; therefore,
we used the Tweedie distribution (Jorgensen, 1987), a family of
exponential dispersion models for positive, discrete, and continuous
data (Dunn, 2014; Smyth, 1996). The Tweedie distribution is useful
for modeling events with a mix of zero and positive observations
(Dunn & Smyth, 2005), like for anchoveta samples obtained by
acoustic methods. The Tweedie distributions are exponential disper-
sion models with a mean and a variance:
EðYÞ ¼ μ and VarðYÞ ¼ φμp ;
where φ is the dispersion parameter and p is an additional parameter
that controls the distribution variance, p ≥ 1 or p ≤ 0.
When p = 0, the Tweedie distribution degenerates to the normal
distribution, When p = 1, the Tweedie distribution becomes a quasi‐
Poisson, and When p = 2, the Tweedie distribution becomes a
gamma distribution.
This function gives an approximate density using the saddlepoint
approximation defined by Nelder and Pregibon (1987). The parame-
ters for the approximate saddlepoint density value for Tweedie
distributions are μ, φ, and power (p). The power index parameter for
CASTILLO ET AL.
the Tweedie distribution (dispersion) was defined using maximum‐
likelihood estimations (MLE). The p maximum values in the summer,
autumn, winter, and spring seasons were 2.13, 2.16, 2.08, and 2.08,
respectively.
The model was fitted by adding explanatory variables one by
one. The error prediction criterion was estimated using the GCV,
and the lowest value indicated the most reliable model. A GAM anal-
ysis was conducted for each season of the year, and an estimated
degree of freedom (edf) was computed for each explanatory variable.
The optimal ranges of the oceanographic parameters with the ancho-
veta distribution were obtained by positive curves of the GAM mod-
els with the intercepts at zero.
2.7 | Environment–resource relationship before and
after the 1997–1998 El Niño event
For these analyses, survey data were separated into two groups (be-
fore and after the 1997–1998 El Niño event). The above‐described
GAM model was used to see whether or not the anchoveta distribu-
tion was related to variations in environmental conditions. Surveys
conducted during the 1997–1998 El Niño event (winter 1997, sum-
mer 1998, and autumn 1998) were not considered in this analysis
(surveys with ONI 1 + 2 values above 2).
2.8 | Software
All analyses were performed using the R Software version 3.3.2 (R
Project for Statistical Computing) packages: “MGCV” version 1.8
(2017), “TWEEDIE” version 2.3 (2017), “GGPLOT2” version 2.2 (2016),
“NCF” version 1.1 (2016), “LATTICE,” and “STATMOD” version 1.4 (2017).
3 | RESULTS
3.1 | Exploratory analysis of anchoveta data:
autocorrelation, seasonal variability, and collinearity
The autocorrelation of anchoveta NASC values is shown by the
residuals of this analysis using an additive model. Here, the residuals
in relation to the years indicated several time intervals with signifi-
cant correlations (Figure 2).
The time series of anchoveta NASC values shows a strong vari-
ability and an asymmetric distribution (Figure 3). Seasonal analyses
F I G U R E 2 Results obtained by an
additive model normalized type of anchovy
NASC values. On the left graph are the
residue residuals of the models, and the
right graph shows the autocorrelation of
the residuals
CASTILLO ET AL. | 5

point to differences in distribution and aggregation levels of the anchoveta and a high spatial dependence (lag) were detected.
schools, and the anchoveta distribution was located closer to the Autumn and spring are transition periods and depend on the magni-
coast in summer (average 16.81 nm) than in autumn (28.77 nm), tude of “normal” or “anomalous” events during summer and winter
winter (27.56 nm), and spring (24.87; Figure 4a). The approach of (Figure 5).
the schools toward the coast in summer causes a higher density or Due to the seasonal variability in the distribution of anchovy,
aggregation, resulting in larger schools per unit area and volume with a GAM was constructed for each season of the year, which
high values of echo integration (NASC average of 1268 m2/nm2). allowed an increase of the explained deviation to diminish the
The opposite was recorded in autumn–winter (NASC average of 525 GCV.
and 715 m2/nm2, respectively) due to dispersion of the schools into The exploratory analysis of the data through pairplots indicated
wider areas (Figure 4b). that the variables “bottom” and “dc” had a high collinearity (0.76), so
An analysis of the spatial distribution of the acoustic data of the bottom variable was not considered in the model. The depth of
anchoveta with geostatistics through variograms showed a high vari- the “bottom” has no influence on the distribution of the anchoveta;
ability for each cruise and even for the seasons of the year. In sum- generally, the schools are found in the surface layer independent of
mer, the statistical sill was high due to greater variances caused by the distance from the coast.
higher concentrations of the anchoveta schools when they moved
toward the coast. This generates short ranges in their spatial depen-
3.2 | Tweedie in GAM
dence as obtained in summer 2006 and summer 2008, while the sill
was low in winter due to the greater dispersion of the anchoveta, Acoustic data included 72.6% of zeros. This pattern of anchoveta
which produces smaller variances with broader ranges compared to distribution in the NASC values, with high amounts of low and zero
summer. In winter 2004, exceptional high concentrations of values, was consistent during all cruises. The distribution of NASC

Factor Autumn Spring Summer Winter

Log(x)

F I G U R E 3 Boxplot of anchovy NASC values (response variable) transformed (logNASC + 1) for the different cruises made between 1985
and 2017. The cruise name is denoted by correlative number of cruise, season, and the last two digits of the year

(a) ● (b) ● ●

●
Average NASC anchovy m2/nm2

50 4,000
Average distance coast (nm)

● ●
40 ● ●
●
●
●
● ●
3,000
● ●
●
●
●
● ●
● ● ●
●
30 ●
●
● ● 2,000 ●

● ● ●
● ● ● ●
● ●
● ● ● ●
● ●
●
● ● ●

F I G U R E 4 Seasonal characteristics of
● ● ● ●
●
20 ●
● ● ● ● ● ●
●
● ●
●
●
●●
● ● ●● ●
● ●● ● ● 1,000 ● ● ●
● ●
●●
the anchoveta distribution. The (a) average ●
●
●
● ●
●
● ● ● ●
●
●
●
●
●
● ● ● ●
●
● ●
●
●
●
● ● ●
● ● ● ● ●●
distance to the coast (nm) and (b) the 10 ● ● ● ● ● ● ●
●
● ● ● ● ●

●
●
●
●
●
● ●
● ● ●
●
●
●
●
● ●

average anchoveta NASC value (m2/nm2)

● ●
0

according to season is presented for all Autumn Spring Summer Winter Autumn Spring Summer Winter

cruises Seasons Seasons

6 | CASTILLO ET AL.

FIGURE 5 Standardized modeling variograms of the anchovy distribution per season for the cruises between 1985 and 2017

values was compared with the Tweedie density for each season (Fig-
3.3.1 | Summer
ure 6). Using the saddlepoint approximation in the Tweedie software
package, the mean of the parameter p is 1.60. The model that best The model for summer explained 35.7% of the deviance, a GCV of
explains the distribution of anchoveta is number V described in 38.72, and an estimation of scale parameters of 525.61 with the
Table 2, which has a lower GCV and a higher explained deviation greatest amount of information. Anchoveta were found at higher
than the other models. It consists of seven covariates: sea surface and wider preferences of sea surface temperature than in the other
temperature (sst), sea surface salinity (sss), dissolved oxygen at the seasons. The temperature model curve (Figure 7a; estimated degrees
sea surface (sso), distance to coast (dc), year, latitude and longitude, of freedom [edf] = 8.956) indicated an optimal temperature for
and Oceanic El Niño Index (ONI 1 + 2). The model in R is as fol- anchoveta between 17.6 and 23.7°C. For sea surface salinity (Fig-
lows: ure 7b; edf = 8.969), the model curve indicates stability up to 35.14
and then decreased with increasing salinity. For sea surface oxygen
gam:anc:tweedieF<-gamðanche sðsstÞ
(Figure 7c; edf = 8.974), the model curve showed a positive trend up
þ sðsssÞ þ sðssoÞ þ sðdcÞ þ sðyearÞ þ teðlong; latÞ þ sðONI:1:2Þ
to 10.2 ml/L with highest abundance of anchoveta between 5.9 and
The explained deviation found by this model increased when 8.7 ml/L. Based on the distance to the coast (Figure 7d; edf = 8.899),
seasonality was considered. anchoveta highly likely occur up to 94 nm off the coast, there is a
zone of reduced abundance in the central part, usually between 35
and 75 nm off the coast. The other variables have been developed
3.3 | Relationship between anchovy and
but are not described due to their minor importance for the scope
oceanographic parameters by season
of this study.
The season‐based models showed certain variations in the
relationship between the anchoveta abundance and the
3.3.2 | Autumn
oceanographic variables (SST, SSS, and SSO; Figure 7, Table 3).
During all seasons, the relationship between anchoveta NASC The model for autumn data explains 29.3% of the deviance, a GCV
values and oceanographic parameters was statistically significant of 33.64, and an estimation of scaling parameters of 231.69 with
(p < 0.001). the least amount of information. The smooth curve for surface
CASTILLO ET AL. | 7

(a) (b) (c)

0.0000 0.0025
Frequency
Frequency
100000

range(fy)
0 15000
Summer
0

0 1,000 2,000 3,000 4,000 5,000 6,000 0 1,000 2,000 3,000 4,000 5,000 6,000 0 1,000 2,000 3,000 4,000 5,000 6,000
Total NASC anchovy Presence NASC anchovy range (y)

Frequency
Frequency

0.000 0.004
range(fy)
15000

3,000
Autumn
0

0
0 500 1,000 1,500 2,000 2,500 3,000 0 500 1,000 1,500 2,000 2,500 3,000 0 500 1,000 1,500 2,000 2,500 3,000
Total NASC anchovy Presence NASC anchovy range (y)

Frequency
Frequency
0e+00 8e+04

range(fy)
0.000 0.003
0 15000
Winter

0 1,000 2,000 3,000 4,000 5,000 6,000 0 1,000 2,000 3,000 4,000 5,000 6,000 0 1,000 2,000 3,000 4,000 5,000 6,000
Total NASC anchovy Presence NASC anchovy range (y)
8e+04

Frequency
Frequency

0.000 0.005
range(fy)
0 10000

Spring
0e+00

0 1,000 2,000 3,000 4,000 5,000 6,000 0 1,000 2,000 3,000 4,000 5,000 6,000 0 1,000 2,000 3,000 4,000 5,000 6,000
Total NASC anchovy Presence NASC anchovy range (y)

F I G U R E 6 Frequency histogram of the response variable anchovy with zeros (a), anchovy without zeros (b), and density using the
dispersion parameter (Tweedie distribution) with the total number of data (c) for each season

temperature (Figure 7e) shows a positive trend up to 21.0°C (edf =
8.844) and a decrease at higher temperatures, which indicates the
absence of anchoveta. Values for surface salinity (Figure 7f; edf =
8.911) lower than 34.52 indicate a lower likelihood of finding
anchoveta with increasing uncertainty for lower values. Stability is
maintained for values between 34.52 and 35.19 with a high proba-
bility of finding anchoveta. For dissolved oxygen (Figure 7g; edf =
8.581), the model shows the presence of anchoveta between 4.3
and 5.8 ml/L with slight fluctuations outside this range. The distance
to coast variable (Figure 7h; edf = 8.962) points to a high probability
of finding anchoveta up to 66 nm off the coast.
3.3.3 | Winter
The model for winter data explained 21.1% of the deviance, a GCV
of 41.49, and an estimate of scaling parameters of 380.69. The sea
surface temperature (Figure 7i; edf = 8.980) showed that the
anchoveta were recorded at lower temperatures than at the other
seasons, with a positive trend up to 18.8°C, indicating absence at
higher temperatures. Sea surface salinity (Figure 7f; edf = 8.953)
shows positive trends at lower salinity values, with a high probabil-
ity of finding anchoveta between 34.81 and 35.12. At higher salini-
ties, a negative decline indicates the absence of anchoveta. The
model curve for dissolved oxygen (Figure 7h; edf = 8.977) generally
shows a positive trend for values below 2.5 ml/L; above 2.5 ml/L, it
slightly decreases and tends to be positive again with a higher like-
lihood of anchoveta being present between 5.2 and 6.3 ml/L. The
model curve for the distance to coast variable (Figure 7l; edf =
8.804) points to stability and high probability of finding anchoveta
up to 90 nm off the coast.
3.3.4 | Spring
The model explained 29.8% of the deviance, a GCV of 32.65, and an
estimate of scaling parameters of 366.53. The smooth curve for the
sea surface temperature variable (Figure 7m; edf = 8.843) indicates a
high probability of finding anchoveta between 15.6 and 19.8°C, and
the probability decreases with a negative trend above and below this
range. For surface salinity (Figure 7n; edf = 8.964), the model curve
indicates a narrow range of probability of finding anchoveta between
34.80 and 35.13, whereas uncertainty is higher for lower salinities.
In relation to dissolved oxygen (Figure 7o; edf = 8.924), the model
curve shows a slightly negative trend below 4.6 ml/L and indicates
an optimal window for the presence of anchoveta between 4.6 and
7.6 ml/L. Above this value, the trend drops to negative values with
increasing uncertainty. Based on the distance to coast (Figure 7p;
edf = 8.981), the model curve is stable and there is a high probability
of finding anchoveta up to 156 nm off the coast.
The variables with the highest probability of finding anchoveta
are summarized in Table 3 for all seasons.
3.4 | Changes in the anchoveta habitat after the
1997–1998 El Niño event
The model applied to cruises before the 1997–1998 El Niño event
explained a deviance of 42.4%, a GCV of 19.82, and an estimate of
8 | CASTILLO ET AL.

T A B L E 2 Model selection results based on GCV and deviance explained values. The model number V was used because its explained deviance was highest and it best described seasonality scaling parameters of 173.88. The surface temperature plot (Fig-

explained
Deviance
ure 8a; edf = 8.806) points to the highest anchoveta NASC values

12.90

21.70

22.90

28.30

29.80
between 14.6 and 21.7°C showing a consistent positive stability;
then, it decreases gradually at higher temperatures. For the surface
40.47 salinity variable (Figure 8b; edf = 8.911), the smooth curve shows a

36.43

35.87

33.35

32.65
GCV

positive relationship for anchoveta at salinities between 34.16 and

35.12; with a negative trend below and above this range, indicating
Intercept
Spring

no presence of anchoveta. The model curve shows decreased nega-

4.44

3.81

3.76

3.24

3.18
tive values from 1.6 to 4.7 ml/L for dissolved oxygen (Figure 8c;
edf = 8.957), indicating no presence of anchoveta at these values.
explained
Deviance

Positive fluctuations occurred between 4.8 and 6.7 ml/L with the
10.60

15.30

19.20

21.10
6.13

highest probability of finding anchoveta. The smooth curve for the

distance to the coast (Figure 8d; edf = 8.962) indicates a high proba-
49.28

46.95

44.46

42.47

41.49
bility of finding anchoveta up to 154 mn off the coast; at further dis-
GCV

tances, a negative trend indicates the absence of the fishes.

Intercept

The model for cruises after the 1997–1998 El Niño event

Winter

explains 20.9% of the deviance, a GCV of 45.37, and an estimation

5.24

5.09

4.89

4.72

4.61

of scale parameters of 536.64 for the greatest amount of informa-

tion. The model curve for surface temperature (Figure 8e; edf =
explained
Deviance

8.839) is almost similar prior to the 1997–1998 El Nino event; the

15.70

18.80

26.80

29.30

interval of the anchoveta distribution was 16.7–23.6°C. The smooth

curve for the surface salinity variable (Figure 8f; edf = 8.918) indi-
40.02

38.57

34.83

33.64

For the autumn season, it was not possible to incorporate the “year” variable in model III due to discontinuity over time.
GCV

cates the highest probability of finding anchoveta between 34.10

and 35.18; then, a decrease was detected at higher salinities, indicat-
Intercept

ing an absence of anchoveta. For dissolved oxygen (Figure 8g; edf =

Autumn

4.05

4.05

3.98

3.61

8.976), the model is negative for lower oxygen values and then
shows a positive trend with the presence of anchoveta between 5.5
and 8.7 ml/L. The distance to coast variable (Figure 8h; edf = 8.909)
explained
Deviance

in the model shows that the anchoveta were found at a distance of

11.70

18.30

21.70

33.70

35.70

up to 108 nm off the coast.

The variables with the highest probability of finding anchoveta
53.15

49.21

47.15

39.95

38.72

Note. Intercept: Parametric coefficient (Estimate). GCV: Generalized Cross Validation.

GCV

before and after the El Niño event are summarized in Table 3.

Intercept
Summer

3.5 | Diagnoses of the GAM

5.28

5.02

4.85

3.93

3.86

According to the diagnostic plots, the anchoveta response variable

with the explanatory variables showed an acceptable residue adjust-
s(sss,bs = ”cr”) + s(sso,bs = ”cr”) + s(dc,bs = ”cr”) + s

s(sss,bs = ”cr”) + s(sso,bs = ”cr”) + s(dc,bs = ”cr”) + s

gam(anch ~ s(sst,bs = ”cr”) + s(sss,bs = ”cr”) + s(sso,

gam(anch ~ s(sst,bs = cr) + s(sss,bs = ”cr”) + s(sso,

ment for the four seasons and for the periods before and after the
s(sss,bs = ”cr”) + s(sso,bs = ”cr”) + s(dc,bs = ”cr”)

s(dc,bs = ”cr”) + s(year,bs = ”cr”) + te(long,lat,

1997–1998 El Niño event. Residue values were widely distributed

along a straight line. The residues in the histogram are normal. The
(year,bs = ”cr”) + te(lon g.lat.bs = ”tp”)

residual with linear prediction, which helps to detect errors not

found in the variance, shows a dispersion at the end only.
bs = ”tp”) + s(ONI,1,2 bs = ”cr”)
Model (variables incorporated)

gam(anch ~ s(sst,bs = ”cr”)+

gam(anch ~ s(sst,bs = ”cr”)+

gam(anch ~ s(sst,bs = ”cr”)+

4 | DISCUSSION

4.1 | Methodological aspects

(year,bs = ”cr”)

bs = ”cr”)+
bs = ”cr”))

In this study, we used GAM models to detect nonlinear relationships

between anchoveta NASC values and oceanographic parameters
combined with a Tweedie analysis due to a mixture of zeros and
positive observations in the data. The advantage of using a Tweedie
Number

distribution in GAM is that it prevents ad hoc modifications of the

IV
III

V
II
I

data (outlier removal), has a non‐negative support and a discrete

CASTILLO ET AL. | 9

(a) (b) (c) (d)

0 15
1 2
0
s(sst,8.96)
)

s(sso,8.97)
s(sss,8.97)

s(dc,8.9)
5
5
(
15

15 20 25 30
sst sss sso dc
(e) (f) (g) (h)
)
s(sst,8.84)
2 0
(
6

(i) (j) (k) (l)

s(sst,8.98)
)
2 0
(
6

(m) (n) (o) (p)

0
)
s(sst,8.84)
2
(
6

F I G U R E 7 a-p show the relationship between anchovy and main oceanographic parameters (temperature, salinity, oxygen, and distance to
the coast) obtained from GAMs computed for the seasons of the years between 1985 and 2017. SST: sea surface temperature (°C), SSS: sea
surface salinity, SSO: sea surface oxygen (ml/L), dc: distance to coast (nm)

T A B L E 3 Range of oceanographic
Season Data DE (%) GCV Scale est. sst (°C) sss sso (ml/L)
parameters with highest probability of
finding anchoveta obtained for each Summer 173,562 35.7 38.72 525.61 17.6–23.7 32.30–35.14 5.9–8.7
season from 1985 to 2017 and before and Autumn 28,583 29.3 33.64 231.69 17.1–21.0 34.52–35.19 4.3–5.8
after the 1997–1998 El Niño event. The Winter 121,184 21.1 41.49 380.69 14.5–18.8 34.81–35.12 5.2–6.3
ranges of the oceanographic variables
Spring 101,932 29.8 32.65 366.53 15.6–19.8 34.80–35.13 4.6–7.6
were obtained from the positive curves of
the GAM graphs with the intercepts at Beforea 60,573 42.4 19.82 173.88 14.6–21.7 34.16–35.12 4.8–6.7
level 0 Aftera 351,098 20.9 45.37 536.64 16.7–23.6 34.10–35.18 5.5–8.7

Note. DE: Deviance explained; GCV: Generalized Cross Validation; Scale est.: Scale parameter
estimation; sst: sea surface temperature; sss: sea surface salinity; sso: sea surface oxygen dis-
solved.
a
Before and after the very strong El Nino event in 1997/98.

mass point in the zero value, and, last but not least, is easy to use in
R. Peel, Bravington, Kelly, Wood, and Knuckey (2012) applied these
models on their fishing data, and Alegre Norza Sior (2011) used it
for the analysis of spatial and temporal relationships in jumbo squid
diet (Dosidicus gigas), both with similar characteristics in the response
variable due to the presence of zeros. Since the Tweedie function
considers only isotropy of spatial data based on the interaction
between smooth tensor products, we suggest that an ideal modifica-
tion of this function would be the incorporation of a command for
spatial autocorrelation for dynamic species to modify the structure
or algorithm in the Tweedie family itself.
Different techniques were implemented for the increasing knowl-
edge about relationships between anchoveta distribution and envi-
ronmental parameters. Castillo (1995), Castillo, Gutiérrez, Vásquez,
and Ganoza (1998), Castillo, Vásquez, Peraltilla, Tello, and Aliaga
(1999), and Segura (2000) used an interpolation technique to calcu-
late the anchoveta distribution and its relationship with temperature
and salinity in the NHCS in 1995–2000. Since the relationships
10 | CASTILLO
(a) (b)
0
s(sss,8.91)
s(sst,8.81)
5
5
15
14 18 22 26
sst sss
(e) (f)
s(sst,8.84)
1
3
sst
F I G U R E 8 Relationship between anchovy and main oceanographic variables (temperature, salinity, oxygen, and distance to the coast)
obtained from GAM, for the periods before (a–d) and after El Niño 1997–1998 (e–h). Periods during the El Niño event (cruises in winter 1997,
summer 1998, and autumn 1998) were not considered. SST: sea surface temperature (°C), SSS: sea surface salinity, SSO: sea surface oxygen
(ml/L), dc: distance to coast (nm)
between anchoveta and oceanographic conditions are likely to be
nonlinear and multivariate, a GAM approach was later used by Ber-
trand et al. (2011), Swartzman et al. (2008), and Gutiérrez, Ramirez,
Bertrand, Morón, and Bertrand (2008) as shown in Table 4.
In summer, 35.70% of the distribution of the anchoveta can be
explained by the variables temperature, salinity, oxygen, distance of
the coast, year, position (latitude, longitude), and ONI 1 + 2. The
explained deviance is 29.8 in spring, 29.3% in autumn, and 21.1% in
winter, indicating that other variables such as winds, currents, phyto-
plankton, zooplankton, chlorophyll‐a, and nitrates. gain importance in
the latter seasons. Unfortunately, long‐term data of such variables
which match with the acoustic data are not available.
4.2 | Ecological aspects
The relationships between anchovy and oceanographic parameters
have been studied by several authors (Table 4). These authors stated
that anchovy tolerates temperatures of 15–24°C, salinities of 34.40–
35.30 and dissolved oxygen values of 3.0–6.0 ml/L. Our results and
other studies showed that these ranges of tolerance change by sea-
son (see Table 4).
Seasonal analysis for anchoveta NASC values revealed different
tolerance ranges for the oceanographic parameters (i.e., SST, SSS
and SSO). Swartzman et al. (2008) established that anchoveta are
strongly linked to CCW and seasonal variations limit the distribution
of this water masses. Also, Segura (2009) and Gutiérrez et al. (2008)
pointed out that salinity is a good indicator to identify this water
masses as SST is more variable (Ganoza, Castillo, & Marin, 2000;
Swartzman et al., 2008). Espinoza and Bertrand (2014) show that
anchovy condition, distribution, and biomass depend on environmen-
tal parameters that vary in different time scales may be influenced
by anomalous events like El Niño. In summer, the anchovy stocks
live closer to the coast as the CCW also gets closer to it. The range
in abiotic parameters preferred by anchoveta is 17.6–23.7°C, 32.30–
ET AL.
(c) (d)
1.5
0
s(sso,8.96)
s(dc,8.96)
0
sso dc
(g) (h)
35.14, and 5.9–8.7 ml/L for oxygen in summer. During winter, it is
14.5–18.8°C, 34.81–35.12, and 5.2–6.3 ml/L for oxygen.
This change in range by season can be influenced by upwelling
processes. In winter, when winds are stronger, the upwelling of cold,
nutrient‐enriched water from deeper layers reduces the SST at the
coast. Also, the plastic adaptability of the anchoveta allows them to
live under different conditions. Various results were found in other
studies in narrower ranges but also in short periods (Table 4). Our
results are similar to those in other studies (Bertrand, Segura, Gutiér-
rez, & Vasquez, 2004; Castillo, 1995; Castillo et al., 1998, 1999;
Gutiérrez et al., 2008 and Segura, 2000) except for Swartzman et al.
(2008) who found optimal ranges in temperature between 14 and
19°C in summer.
4.3 | Changes after the 1997–1998 El Niño event
The hydroacoustics evaluation started in Peru in 1983 (1985 for
anchoveta) and indicated that the most abundant pelagic resources
were anchoveta, sardine, jurel, and mackerel. These four species
usually share the distribution areas with high levels of biomass (3–
4 million tons on average off Peru). The impact of the very strong
El Niño event in 1997/1998 created differences in the Peruvian
Current ecosystem with a reduction in biomass and distribution of
these main pelagic species except for anchoveta (Gutiérrez et al.,
2012).
Our analysis showed that the preferred abiotic parameters of
anchoveta changed after the 1997–1998 El Niño event. Anchoveta
were preferably found at temperatures between 14.6 and 21.7°C
before the El Niño event and from 16.7 to 23.6°C after the event.
Similar changes occurred in salinity and dissolved oxygen. This
change could be related to the change of the PDO (Pacifical decadal
oscillation), since the NHCS was in a warm period before the El Niño
event and in cold period after that event. Gutiérrez et al. (2011)
already stated that the sea surface temperature in the Pacific Ocean
CASTILLO ET AL. | 11

T A B L E 4 Results of other studies on the relationships between anchovy and oceanographic parameters
Optimal
temperature Optimal Optimal
Period Data type Method (°C) salinity oxygen (ml/L) Source
Summer Acoustic, oc eanographic and Overlaying graphics generated by 15–21 34.85– Castillo
1992 fishing hauls data interpolation 35.10 (1995)
Summer
1993
Summer
1994
Autumn Acoustic and oceanography Overlaying graphics generated by 17–22 34.90– Castillo et al.
1998 data interpolation 35.20 (1998)
Summer Acoustic and oceanography Overlaying graphics generated by 17–22 (2– 34.40– Castillo et al.
1999a data interpolation (layers) 10 m) 35.20 (1999)
18–21 (10– 34.90–
25 m) 35.30
15–22 34.60–
(transects)b 35.25
1986– Acoustic data with satellite Acoustics graphics overlaying with <23 <35.20 Segura (2000)
2000 information satellite images
1997– Acoustic and oceanography GAM (bivariate models) with S‐plus (log 16–24 34.90– 3.0–4.5 Bertrand
1999 data transformed sA of anchovy) 35.00 et al. (2004)
1983– Acoustic and oceanography GAM binomial distribution with S‐plus Spring: 14–18 34.80– Swartzman
2005 data function Step.gam Summer: 14– 35.05 et al. (2008)
19
Autumn‐
winter: 14–
18
1998– Acoustic and oceanography GAM with S‐plus (log transformed sA of 14–23 34.70– 4.0–6.0 Gutiérrez
2006 data anchovy) 35.10 et al. (2008)

Note. sA: values of anchoveta integration in m2/nm2. Cruise conducted after 1997–1998 El Nino event.
a
Cruise conducted after 1997–1998 El Niño event. bOnly in six hydrographic transects.

and the thickness of the oxygen minimum zone increased after the
1997–1998 El Niño event. Such changes in ecosystem conditions
are considered to be favorable for anchoveta because its habitat
increases (Bertrand et al., 2011). Bertrand et al. (2004) and Gutiérrez,
Swartzman, Bertrand, and Bertrand (2007) suggested that anchoveta
adopted a space refuge strategy during the 1997–1998 as a protec-
tive mean against unfavorable environmental conditions. Forced by
the biological need to adapt to changing ecosystem conditions and
fostered by the absence of other pelagic species, anchoveta had a
wider area of expansion (Bertrand et al., 2004). Moreover, the
absence of these pelagic species during the El Niño event allowed
an increase in the population of Pleuroncodes monodon, a crustacean
known as red squat lobster (Gutiérrez et al., 2008).
The 2015–2016 El Niño event started in autumn of 2015 and
was considered by the ENFEN (National Study of “El Niño”) with an
event of magnitude “strong,” which reached its maximum intensity in
December 2015 with strong anomalies of the Superficial Tempera-
ture of the Sea on the Pacific coast, producing only a migration of
the anchoveta toward the south and toward the coast. After this
event, the distribution normalized without substantially affecting the
anchoveta abundance.
5 | CONCLUSIONS
This is the first time that a long‐term period of anchoveta distribu-
tion (32 years of data) is presented in which we could analyze the
behavior of its distribution under different seasonal conditions. The
environmental tolerance of anchoveta changes with season. In sum-
mer, the anchovies were mainly detected at temperatures between
17.6 and 23.7°C, salinities between 32.30 and 35.14 and oxygen
levels between 5.9 and 8.7 ml/L. In winter, temperatures between
14.5 and 18.8°C, salinity between 34.81 and 35.12, and oxygen
levels between 5.2 and 6.3 ml/L were preferred. Wider tolerances
were observed in summer compared to other seasons. In addition,
after the 1997–1998 El Niño event, the anchoveta were detected at
higher ranges in temperature, salinity, and dissolved oxygen.
The capability of anchoveta to cope with seasonal changing envi-
ronmental conditions and to survive during El Niño events guaran-
tees their continuity in the ecosystem. This plasticity and adaptation
of the anchoveta to environmental changes is known since the
beginning of its capture in the 1950s and has maintained its abun-
dance, survival, and growth. The Pacific decadal oscillation (PDO)
and climatic change are probably the influencing factors in
12 | CASTILLO
environmental dynamics. This result can be used in predictive models
for anchoveta distribution and abundance.
ACKNOWLEDGEMENTS
The authors thank the researchers working in the IMARPE Hydroa-
coustic Laboratory between 1983 and 2017 for their dedication,
efforts, and responsibility. Many of them—Adolfo, Mariano, Gabriel,
Salvador, Aníbal, Hector, Giuliana, Dora, Gloria, Noemi, and others—
are now working elsewhere.
CONFLICT OF INTEREST
The authors whose names are listed immediately below certify that
they have NO affiliations with or involvement in any organization or
entity with any financial interest, or non‐financial interest in the sub-
ject matter or materials discussed in this manuscript.
ORCID
Ramiro Castillo http://orcid.org/0000-0003-0580-2742
Rolf Koppelmann http://orcid.org/0000-0002-0561-9617
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How to cite this article: Castillo R, Dalla Rosa L, García Diaz
W, et al. Anchovy distribution off Peru in relation to abiotic
parameters: A 32‐year time series from 1985 to 2017. Fish
Oceanogr. 2018;00:1–13. https://doi.org/10.1111/fog.12419