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Stable isotope analysis reveals pelagic foraging by the Southern sea lion in
central Chile

Article  in  Journal of Experimental Marine Biology and Ecology · August 2007

DOI: 10.1016/j.jembe.2007.03.014

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 Journal of Experimental Marine Biology and Ecology 347 (2007) 123 – 133
www.elsevier.com/locate/jembe

Stable isotope analysis reveals pelagic foraging by the

Southern sea lion in central Chile
L.A. Hückstädt a,b,⁎, C.P. Rojas b , T. Antezana b
a
Ocean Sciences Department. University of California Santa Cruz. Long Marine Lab, 100 Shaffer Road, Santa Cruz, CA 95060, USA
b
Departamento de Oceanografía. Universidad de Concepción, Casilla 160-C, Concepción, Chile
Received 16 March 2007; accepted 27 March 2007

Abstract

The diet of Southern sea lion Otaria flavescens is poorly known along the coast of central Chile (32°–39°S), where a
population of about 17,300 individuals occurs, in an ecosystem that sustains one of the world's most important fishing industries.
The primary objective of this study was to reconstruct the diet and estimate Trophic Positions (TPs) of sea lions and their prey off
central Chile using stable isotopes (δ13C and δ15N). Our results showed that the diet of sea lions is primarily composed of pelagic
prey, with the jack mackerel Trachurus murphyi as the principal prey item in the diet of sea lion (1–99th percentile: 20–66%),
while demersal prey accounted for only 0–2.8%. We also found regional differences on the relative contribution of prey to the diet
of sea lions. Animals that were sampled close to major fishing areas showed an increase in the relative contribution of jack
mackerel to the diet as opposed to animals sampled away from these areas that displayed a relatively more heterogeneous diet.
Trophic Positions (TPs) of sea lions prey items ranged between 3.39 for jack mackerel and 4.48 for pink cusk-eel (Genypterus
blacodes). The TP for sea lions was 4.57. Hence, our results showed a community composed by at least 5 trophic levels, with sea
lion as the top predator. In summary, our study demonstrates that the Southern sea lion is displaying pelagic foraging off central
Chile. We highlight the necessity of conducting further research on the trophic ecology and diving behavior of Southern sea lion to
obtain a better understanding of their role as top predator.
© 2007 Elsevier B.V. All rights reserved.

Keywords: Diet; Marine mammal; Otaria flavescens; Prey; δ13C; δ15N; Trophic level

1. Introduction lion (Otaria flavescens) has not been studied along its
Pacific range, but some information is available from
Most sea lions species have been traditionally char- studies conducted in Argentina on females (Campagna
acterized as benthic foragers, with the exception of the et al., 2001; Thompson et al., 1998; Werner and Cam-
California sea lion Zalophus californianus, which dis- pagna, 1995). Off the Argentinean coast, Southern sea
plays an epi- or mesopelagic diving behavior (Costa lions forage on the shelf, although dives of N300 m have
et al., 2004). The diving behavior of the Southern sea been recorded (Thompson et al., 1998). This diving
pattern is likely to be related to the depth of the con-
tinental shelf off Argentina. For instance, the range of
⁎ Corresponding author. Tel.: +1 831 459 3112; fax: +1 831 459 the deepest dives recorded for female Southern sea lion
3383. (N60 m) is similar to the depth of the shelf in that area
E-mail address: [email protected] (L.A. Hückstädt). (Campagna et al., 2001).
0022-0981/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2007.03.014
124 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133

One should expect significant differences in the div- erel (Trachurus murphyi), hake (Merluccius gayi) and
ing behavior of Southern sea lion foraging along the anchovy (Engraulis ringens) (Aguayo-Lobo et al., 1998;
Atlantic and Pacific coasts, particularly if we consider George-Nascimento et al., 1985). All of these prey items
the striking differences between the two systems. For are commercially exploited by local fisheries, resulting in
instance, the continental shelf off Argentina is consid- conflicts between sea lions and commercial and minor-
erably wider (up to 400 km) than the shelf off Chile scale fisheries (Aguayo and Maturana, 1973; Hückstädt
(b66 km in central Chile), and thus we would not nec- and Antezana, 2003; Oporto et al., 1991).
essarily expect foraging to be associated with the shelf The most common method used to reconstruct diets
as has been suggested for Argentinean waters (Hück- of pinnipeds is the identification of prey remains
städt and Krautz, 2004). collected from stomachs, intestines, scats and regurgita-
The Southern sea lion is the only species of pinniped tions (Tollit et al., 2003). This approach presents several
regularly inhabiting the coast of central Chile (32°–39°S), advantages, such as its low cost and the high likelihood
where a population of 17,300 individuals has been esti- of finding samples with identifiable prey (Bowen and
mated (Aguayo-Lobo et al., 1998). The information Siniff, 1999; Hammill et al., 2005). Yet, the accurate
available on diet of the species in Chile is limited and reconstruction of diet using this method is complicated
mostly out of date (Hückstädt and Antezana, 2006). Al- by erosion and differential digestion of hard parts, and
though the species has been historically considered an also a high proportion of samples with no prey remains
opportunistic predator with a broad diet spectrum for its (Bowen, 2000; Bowen and Siniff, 1999; Naya et al.,
Atlantic range (Koen-Alonso et al., 2000; Naya et al., 2000).
2000), it appears that Southern sea lion along the Chilean Naturally occurring isotopes of Carbon (C) and Nitro-
coast feeds on a lower diversity of prey items (Hückstädt gen (N) are increasingly used to study trophic relation-
and Antezana, 2006). ships and feeding habits of marine mammals, based on the
Studies conducted on the diet of Southern sea lions off idea of a relatively consistent and predictable relationship
central Chile in the early 80s and late 90s indicate that between predator and prey (Hobson et al., 1996; Lesage
they fed mainly on Patagonian grenadier (Macruronus et al., 2001; Phillips, 2001; Post, 2002; Vander Zanden
magellanicus), cusk-eel (Genypterus spp.), jack mack- and Rasmussen, 2001). Stable isotopes are also used in

Fig. 1. Study area at the marine ecosystem off central Chile. The dots correspond to the locations where Southern sea lion samples were obtained for
stable isotopes analysis and the number of samples for each location is also indicated. The isobath of 200 m represents the break of the continental
shelf.
 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133 125

studies of food webs based on the fact that isotopes either Table 1
fractionate or change in a predictable fashion between δ13C and δ15N values for Southern sea lion and its prey off central
Chile
trophic levels and so reflect trophic position.
Dietary studies using stable isotopes provide a longer n δ13C (‰) δ15N (‰)
record than traditional methods, indicating that the prey POM N/A − 21.60 8.88
has not only been ingested, but also assimilated, and Crustacea
Humboldt krill 30 − 16.04 a 12.37
unlike stomach or scat analysis, all sampling efforts
Mollusca
yield information (Bowen and Siniff, 1999; Burton and Jumbo flying squid 3 − 15.06 18.52
Koch, 1999; Hobson et al., 1996; Kurle and Worthy, Chondricthyes
2001; Lesage et al., 2001). On the other hand, this Elephant-fish 4 − 13.63 19.20
method does not allow for the identification of the Osteichthyes
Anchovy 15 − 15.56 17.83
species that are being consumed, and therefore pre-
Black cusk-eel b 5 − 13.90 20.71
vious knowledge of potential prey sources is necessary Pink cusk-eel b 6 − 13.68 20.71
(Hobson et al., 1996; Post, 2002; Vander Zanden and Red cusk-eel b 3 − 13.87 18.47
Rasmussen, 2001). Hake 6 − 14.42 17.67
Here we present a novel analysis on the diet of the Jack mackerel 5 − 16.07 17.02
Grenadier 6 − 15.02 20.12
Southern sea lion in the central coast of Chile based on the
Herring 2 − 14.71 17.67
analysis of stable isotope ratios (δ13C and δ15N). Ad- Mammalia
ditionally, we present a first insight to the trophic structure Sea lion c 27 − 12.48 ± 0.68 20.97 ± 0.77
of the coastal ecosystem off central Chile, based on the Values for the Humboldt krill and Particulate Organic Matter (POM)
abundances of δ13C and δ15N from Southern sea lion, are also included.
previously reported sea lion prey items, Humboldt krill a
Carbonate enrichment factor (0.4‰) applied to δ13C value.
b
and Particulate Organic Matter (POM). Previous studies on the diet of sea lion did not make distinctions
among the three species of the genus Genypterus spp.
c
Values ± SD.
2. Materials and methods

2.1. Collection and analysis of samples Samples were then homogenized and preserved at
− 18 °C. Humboldt krill Euphausia mucronata samples
We sampled hair and vibrissae from 27 Southern sea of abdominal muscle were obtained from plankton
lions found dead along the central Chile coast (n = 7), or collected in spring 2002 within the CSUR, homoge-
incidentally caught during fishing operations of both nized and preserved at − 18 °C until analysis. POM was
minor-scale (n = 19) and commercial fishing fleet (n = 1) obtained from water collected using Niskin bottles at
between November 2001 and October 2002 (Fig. 1). 8 m depth (depth of Chlorophyll maximum) in spring
We only sampled freshly dead animals without exterior 2002 at 36°20′ S and 73°44′ W. The sample was then
signs of diseases or injuries. filtered through Whatman GF/C filters (1.2 μm).
Hair samples were collected by extracting a section
of ca. 2 cm2 of skin and hair with a scalpel, followed by 2.2. Chemical analyses
removal of the skin. Vibrissae were extracted entirely
from the root. Samples were preserved at − 18 °C until Hair and vibrissae samples were washed with dis-
analysis. Location and date of sampling were recorded tilled water and soap at least five times. Samples were
for each sample. Information on morphometrics and sex then rinsed with ether petroleum to extract remaining
was available for only eight individuals (all males). lipids (Kurle and Worthy, 2002), followed by a second
Ten sea lion prey species were selected for analysis washing with distilled water again and dried at 60 °C for
based on the last information available on diet com- 48 h.
position of sea lion in central Chile (Aguayo-Lobo et al., A study conducted in an otariid, the Steller sea lion
1998; George-Nascimento et al., 1985; Hückstädt and Eumetopia jubatus, demonstrated that sea lions exhibit
Antezana, 2006) (Table 1). Samples were collected a consistent growth and year-to-year retention of their
directly from fisheries landings conducted within the vibrissae, with average growth rates of 0.11–0.12 mm/
Central-Southern Upwelling Region (CSUR) of the day (Hirons et al., 2001), while the hair is molted
Humboldt Current System (HCS) during the austral annually. Vibrissae samples were thus analyzed for the
spring, 2002. A section of ∼ 1 cm3 of muscle per indi- first centimeter from the base, allowing us to examine
vidual was collected using a scalpel. the diet of the sea lions during the last year or 2 months,
126 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133

and making it comparable to the isotopic data collected www.epa.gov/wed/pages/models/stableIsotopes/iso-

from the hair. source/isosource.htm). The IsoSource model provides a
Muscle samples from all prey items and Humboldt formalized, general procedure by which ranges of
krill were treated to extract lipids (Bligh and Dyer, source contributions can be determined when the num-
1959), due to the fact that lipids are ∼ 6‰ lighter in ber of sources is too large to permit unique solutions
δ13C relative to proteins, adding variability to δ13C from stable isotope mixing models (Hall-Aspland et al.,
values (Lesage et al., 2001). After this process, muscle 2005; Phillips, 2001).
samples were dried at 60 °C for 48 h prior to isotopic A first analysis was conducted including 10 prey
analyses. items identified for the species. For this analysis source
POM samples were washed with HCl 0.12 N to elim- increments of 2% and a mass balance tolerance of ± 0.04
inate carbonates, which may add undesirable variability to were set. Based on these results, we determined a cutoff
δ13C (Lorrain et al., 2003). Carbonates may also inflate of 10% of the relative contribution of jack mackerel to
the δ13C values of invertebrates by about 0.4‰, but the diet of sea lion (jack mackerel mean relative con-
treatment with hydrochloric acid adversely affects δ15N tribution to the diet of sea lion was 49.3%), following a
(Bunn et al., 1995; Jardine et al., 2003; Lesage et al., criteria similar to that applied by Ben-David et al. (2004)
2001). Therefore, a correction factor of 0.4‰ was used for for brown bears.
the δ13C of krill. We conducted a second analysis with IsoSource,
The abundance of stable isotopes is expressed in including only those items whose relative contribution
delta (δ) notation using Eq. (1): to the sea lion diet was above the cutoff value. For this
analysis, source increments of 1% and a mass balance
Rsample  Rstandard tolerance of ±0.02 were set.
dX ¼  1000 ð1Þ
Rstandard The dissimilarity in diet composition between
locations (i.e. Cobquecura and Talcahuano-San Vicente)
where δX is the difference in the isotopic composition was estimated using mean prey contributions to the diet,
between the sample and the standard in parts per as obtained from IsoSource. Two indexes were used as
thousand (‰), and R is the ratio between the heavier indicators of dissimilarity of diet:
and lighter isotope (i.e. 13C/12C, 15N/14N). The standard
for δ13C corresponds to PeeDee Belemnite (PDB), and 1. Euclidean distance (Δjk) between locations:
the standard for δ15N is atmospheric nitrogen.
Samples were analyzed using a mass spectrometer sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
X n  2
Thermo Finnigan Delta Plus coupled with an elemental Djk ¼ Xij  Xik ð2Þ
analyzer Thermo Finnigan Flash EA 1112 (PROFC, i¼1
Universidad de Concepción). The analytical error for
sea lions samples was ± 0.02‰ and ± 0.36‰ for δ13C where Xij is the proportion of species (prey) i in sample
and δ15N, respectively. The analytical error for all other (location) j, Xik is the proportion of species i in sample
samples was ± 0.05‰ and ± 0.13‰ for δ13C and δ15N, k, and n is the total number of prey species.
respectively. 2. Levin's index of niche breadth (B) for sea lion at each
location:
2.3. Data analyses
1
B¼P 2 ð3Þ
All data were tested for normality using the Kolmogorov– pj
Smironov test. The isotopic values of sea lion were corrected
using tissue-specific Trophic Enrichment Factors (TEFs) where pj is the proportion of the prey j in the diet.
determined for pinnipeds (Hobson et al., 1996). Differences
for the corrected isotopic values between hair and vibrissae To estimate the Trophic Position (TP) for all species
samples were examined using t-tests, as well as the dif- except the sea lions, δ15N values were converted as
ferences between the two sampling locations Cobquecura follows:
and Talcahuano-San Vicente (Fig. 1). Significance was
tested at the α = 0.05 level. Power was calculated for tests TP ¼ 1 þ ðDm  POMÞ=TEF ð4Þ
at the specific sample size and α = 0.05.
The contribution of the prey items to the sea lions diet where Dm =δ15N value for a consumer, POM=δ15N value
was estimated using the software IsoSource 1.3.1 (http:// of Particulate Organic Matter (POM), and TEF = trophic
 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133 127

Table 2
Contribution of prey items to the diet of Southern sea lion in central
Chile
Prey item Contribution to the diet
1–99 percentiles (%)
Jack mackerel 20–66
Anchovy 0–58
Herring 0–20
Grenadier 8–26
Squid 0–26
Hake 0–8
Elephant-fish 0–8
Black cusk-eel 0–12
Pink cusk-eel 0–12
Red cusk-eel 0–8
Fig. 2. Mixing polygon for δ13C and δ15N signatures of prey items (●)
and Southern sea lions (○) in central Chile. Values are shown as 1–99 percentiles for the corresponding distributions.

enrichment factor in δ15N. TEF is typically assumed as isotopic signature) falling near the end dominated by
3.4‰ (Vander Zanden and Rasmussen, 2001). pelagic prey (Fig. 2).
For the sea lion, TP was estimated using Eq. (5) With all 10 prey items included in the analysis, jack
(Lesage et al., 2001). mackerel appeared as the primary food source (1–99th
percentile: 20–66%), followed by anchovy (0–58%).
TP ¼ 2 þ ðDm  POM  TEFmmt Þ=TEF ð5Þ Demersal prey items (hake, cusk-eels, and elephant-fish
Callorhynchus callorhynchus) were minor components of
where TEFmmt = tissue-specific trophic enrichment the diet (only 0–2.8% of the diet) (Table 2).
factor in δ15N calculated for pinnipeds (Hobson et al., When we conducted the analysis with the four main
1996). prey items selected after the cutoff, the figures changed.
Anchovy appeared now as the most important prey item,
3. Results although its distribution of feasible diet proportion was
not well constrained (0–88%).
3.1. Descriptive analysis Jack mackerel was now the second most important
prey item (3–49%), followed by jumbo flying squid
The values of δ13C and δ15N for sea lion ranged Disodicus gigas (0–40%) and grenadier (7–15%).
between − 14.92 and − 11.43‰, and between 19.75 and However, when we considered only four prey, the dis-
23.45‰, respectively (Table 1). The δ13C and δ15N tributions of feasible diet proportion were not well con-
values for sea lion were normally distributed (Kolmo- strained, limiting our analyses.
gorov–Smironov, all p N 0.05). The values of δ13C and
δ 15 N for prey items ranged between − 16.07 and
− 13.63‰, and between 17.02 and 20.71‰, respectively
(Table 1).
When analyzing differences in isotopic values
between tissues we found no significant differences
for δ13C (t = 1.03, p N 0.05, power = 0.17) nor for δ15N
(t = 1.75, p N 0.05, power = 0.39). Similarly, we found no
differences in isotope signatures between sampling
location for δ13C (t = − 1.25, p N 0.05, power = 0.23) or
δ15N (t = − 0.40, p N 0.05, power = 0.07). In all cases, the
statistical power was low to detect an effect.

3.2. Sea lion diet

Fig. 3. Difference in the mean contribution of prey items to the diet of
The mixing polygon of sea lion prey items was southern sea lion between the locations of Cobquecura (n = 19) and
relatively broad (Fig. 2), with the mixture (sea lion Talcahuano-San Vicente (n = 5), central Chile.
128 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133

3.3. Differences in the diet of sea lions between Table 3

locations Trophic Positions (TPs) of preys included in the diet of southern sea
lion estimated from δ15N and reported stomach content data a

The diet of sea lions from Cobquecura was domi- Prey TPδ15N TPstomach content data

nated by jack mackerel, followed by anchovy (Fig. 3). Jack mackerel 3.39 3.56–3.82
There is also a slight increase in the importance of non- Hake 3.59 4.26
Herring 3.59 2.69
pelagic items with respect to the overall data. The diet of
Anchovy 3.63 2.70–2.86
sea lions from Talcahuano-San Vicente was dominated Red cusk-eel 3.82 ND
by jack mackerel, whose importance in the diet of sea Jumbo flying squid 3.84 ND
lion increased with respect to Cobquecura, followed by Elephant-fish 4.03 3.23–3.45
the grenadier (Fig. 3). Patagonian grenadier 4.31 3.93
Black cusk-eel 4.32 ND
The Euclidean distance of the diet of sea lion between
Pink cusk-eel 4.48 4.18–4.34
locations was 30.3%. The analysis of Levin's niche breadth
ND = no data found.
(B) for each location revealed a relatively more generalistic a
Obtained from FishBase (http://www.fishbase.org).
strategy for sea lions from Cobquecura (BCobquecura =4.1),
while sea lions from Talcahuano-San Vicente displayed a
narrower niche (BTalcahuano-San Vicente =1.99).
pink cusk-eel G. blacodes, followed by the black cusk-
3.4. Ecosystem structure and TPs eel G. maculatus and the grenadier (Table 3).

The δ 13 C varied by 9.21‰ between POM and the 4. Discussion

sea lions, while the δ15 N varied by 11.94‰ (Table 1).
The δ 13 C for fishes ranged between − 16.07 and Understanding of the diet of Southern sea lion along
− 13.63‰, and the δ15N ranged between 17.02 and the Chilean coast has until now relied on limited
20.71‰. Two carbon pathways which the sea lion research conducted 20 years ago (George-Nascimento
partake in could be identified based on the δ 13 C values: et al., 1985). Ours is the first published assessment of the
the demersal or benthic pathway was represented by diet of southern sea lions off central Chile since the
species with higher δ 13 C values, while species repre- 1980s, and the first to assess the trophic position of sea
senting the pelagic pathway had lower values of δ13 C lions and their prey.
(Fig. 4). Unfortunately, we had no information on morpho-
The TPs varied between 2 for Humboldt krill and metrics, age, and sex classes from most of the
4.57 for sea lions. The TPs of fishes ranged between individuals included in this study, limiting the analyses
3.47 and 4.48, and the TP of squid was 3.84. The highest that could be conducted in our study. However, as all
TP among the sea lion's prey items was occupied by the unidentified samples came from fisheries by-caught
animals, it is highly likely that they corresponded to
males individuals, given that: (1) males interact
predominantly with fisheries, at an approximate ratio
of 3:1 ratio over females (Hückstädt and Krautz, 2004;
Koen-Alonso et al., 2000), (2) males feed mainly on
pelagic items (Oliva, 1984). Additionally, all animals
whose sex was recorded were male. Therefore, the diet
description presented in this study is more likely to
correspond to males alone rather than the entire
population of Southern sea lions off central Chile. We
also acknowledge the potential bias towards diet
corresponding with fisheries in which some animals
were by-caught.
The isotopic analysis of metabolically inactive tissue
such as hair and vibrissae yields information on the diet
Fig. 4. Trophic Position (TP) of southern sea lion (▲) and its prey in
integrated over a time scale of months. This is a
central Chile. The black dots indicate pelagic prey. Open circles comparative advantage with respect to studies of
correspond to demersal prey. metabolically active tissues that provide information
 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133 129

limited to time scales of days to weeks, and stomach Although vibrissae and hair of pinnipeds are similar
contents and scat analyses studies, which present only in biochemical composition, there are considerable
an instantaneous view of diet (Hall-Aspland et al., 2005; differences between both tissues: vibrissae are large
Hobson et al., 1996). overall, highly innervated, present large blood sinuses

Fig. 5. Comparisons of prey contributions to the diet of southern sea lion (bars) as obtained from George-Nascimento et al. (1985) and 2002 (this
study). The data from 1980s correspond to % mass obtained from stomach analyses. The solid line corresponds to fish landings. (Source: Servicio
Nacional de Pesca, Chile).
130 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133

and are controlled by voluntary muscles (Hirons et al., 1985; Hückstädt and Antezana, 2006; Koen-Alonso
2001), while hairs present a central cavity or medulla et al., 2000), it is expected that the change in diet would
and lack erector pili muscles (Berta et al., 2006). These reflect changes in the environmental availability of prey.
differences in the structure could be indicative of Nonetheless, it is important to keep in mind this
different isotopic enrichment factors for each tissue. apparent shift in diet may also simply be a result of
Studies conducted with animals in captivity indicated a differences in time scales covered by the two method-
higher enrichment in δ13C for vibrissae in comparison ologies, as our samples reflect prey items that were
to hair (+ 3.2‰ versus + 2.8‰) (Hobson et al., 1996), consumed by sea lions on a scale of weeks to months,
while δ15N enrichment showed low variability among and previous studies reflect items consumed on a scale
high-protein tissue. Our results revealed no signifi- of hours to days.
cant differences in the δ13C and δ15N values between Due to the lack of information available on the
tissues. variations of prey biomass, we used fish landings as a
The analysis between sampling locations showed no proxy for environmental availability of prey and
significant differences for both isotopes, although a examined our results in light of these changes. However,
relatively higher mean value was observed at Cobque- it is necessary to assume that changes in fish landings
cura, likely associated to a particular individual with a are related to changes in the availability (i.e. biomass) of
δ15N of 23.45‰. Changes in the nitrogen isotopic com- the resource in the environment (Fig. 5), which might be
position of animal tissues can be used as indicators of done to some extent.
change in body condition (Gannes et al., 1997; Kelly, The main change in the diet is related to the increase
2000; Vander Zanden and Rasmussen, 2001), and this in importance of jack mackerel in the diet of sea lions
high value could be an indicator of starvation. On the (Fig. 5). Landings of this species rose continuously from
other hand, the relatively lower values of δ15N found in ca. 600,000 tons in 1979 to a historical maximum of
animals from Talcahuano-San Vicente could be a re- 4.4 million tons in 1995, and then decreased and sta-
flection of the better condition of animals at this location. bilized at about 1.5 million tons after 1999, reaching
At Talcahuano-San Vicente animals are exposed to a 1.5 million tons in 2002. Anchovy was not reported in
continuous and easily accessible food supply from the diet 20 years ago, but in this study it was the second
discards from fishing vessels and fish processing plants most important prey for the sea lions. The landings of
in the area, largely dominated by jack mackerel. this species have been erratic, with important interannual
variations, yet an increasing trend is evident from the
4.1. Diet of sea lions early 1980s with landings of few thousand tons per year
(e.g. 300,000 in 1981) to a historical maximum of
The contribution of prey items to the diet is possible 2.7 million tons in 1994. This species also experienced a
to model using isotopic analyses only if the diet is decrease of its landings to about 1.5 million tons in 2002.
heterogeneous, being dominated by a few prey items Herring (Strangomera bentincki) was not previously
(Hammill et al., 2005; Phillips, 2001). Analyses of niche reported in the diet (George-Nascimento et al., 1985).
breath of Southern sea lion along the Chilean coast Landings of herring were about 20,000 tons during the
indicate that its diet is dominated by few species, likely 1980s, and during the 1990s landings increased to the
associated to the environmental dominance of resources order of 300,000–500,000 tons, and 350,000 tons
such as anchovy and jack mackerel (Hückstädt and were landed in 2002. On the other hand, the sardine
Antezana, 2006). (Sardinops sagax) corresponded to 4.8% mass of the diet
A recent study on harp seals (Pagophilus groenlan- in the 1980s but it was not included in this analysis since
dicus) highlighted similarities in diet reconstruction it is not reported to occur in the area today. Grenadier
using stable isotopes and stomach contents (Hammill decreased in importance in the diet of sea lions, but this is
et al., 2005). Given these results and George-Nasci- not reflected in the landings of the species which,
mento et al. (1985) study on diet of Southern sea lions oppositely, increased between the 1980s and 2002. The
using stomach contents, we can hypothesize about a squid increased from 0.8% mass to 8.3%, but no
significant shift in the last 20 years from a diet dom- information on landings of the squid was available.
inated by demersal prey to one dominated by pelagic The contribution of demersal prey to today's diet of
prey (up to 91% of the diet), as is evident from the δ13C sea lion was low, with an overall contribution of less
results for prey (Fig. 4). than 9% to sea lion diet.
Since the Southern sea lion is a plastic predator Although the figures presented in this analysis match
(Aguayo and Maturana, 1973; George-Nascimento et al., in general terms, this is intended only as a broad
 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133 131

analysis, and should not be considered as a direct cor- fishes included in this study (jack mackerel, anchovy,
relation between the fisheries trends and the diet of sea herring and grenadier), and the squid, displayed a mean
lions. It is unknown if the diet of sea lion reflected the TP of 3.75, while the demersal or benthic species had a
trends in the fisheries during the entire period, as there is higher mean TP (4.04). Some differences were found
no concurrent time series data of sea lion diet when the values obtained from this study were
composition available. contrasted with dietary TP estimates based on stomach
Even though no significant differences were found content data available online (http://www.fishbase.org).
for the isotopic values between locations, the power of The black cusk-eel and jack mackerel showed similar
all these analyses were low. Therefore, differences in values to those reported based on stomach contents data.
diet of sea lions between locations might still be ex- The elephant-fish and anchovy had higher TPs than
pected. This was confirmed with our estimation of those previously informed, while hake showed a lower
Euclidean distance and niche breath for each location. TP (Table 3). Although δ15N is highly variable among
The distance and difference in niche breadth between systems, its use as an estimate of TP provides a time
locations was attributable to the higher proportion of integrated measure of an organism's TP, and accounts
jack mackerel in the diet of animals from Talcahuano- for temporal and spatial variation in feeding, while the
San Vicente compared with animals from Cobquecura. dietary data provides only a snapshot in time and
Although the niche breadth analysis revealed animals presents high variability associated with the estimates of
from Talcahuano-San Vicente as more specialized, the prey TPs (Vander Zanden et al., 1997).
dominance of jack mackerel in the diet of these The stable isotope analyses revealed clear distinc-
animals could be reflective of the “free-food” condi- tions between the pelagic and demersal carbon pathways
tion in that particular location, as discards from jack in central Chile, with sea lions participating principally
mackerel’ fishing vessels and plants are available to in the pelagic system. As expected, sea lions occupied
sea lions. the role of top predator in the ecosystem but its influence
on the dynamics and structure of the ecosystem remains
4.2. Community structure unknown. The use of stable isotopes proved valuable to
approach the diet of sea lions and the structure of the
The central Chile community consisted of at least ecosystem off central Chile; however the analyses of the
five trophic levels, with the sea lion as the top predator data obtained and comparisons are limited by the lack of
(TP = 4.57). This value is similar to TPs reported for other studies on the species.
other pinniped species in the North Atlantic (Lesage Members of the family Otariidae (sea lions) have
et al., 2001). Alternatively, killer whales Orcinus orca been traditionally characterized as benthic foragers, with
have been proposed to predate on marine mammals in the exception of the California sea lion, which displays
this area or, at least, on sea lions (Hückstädt and an epi- or mesopelagic diving behavior (Costa et al.,
Antezana, 2004), which would imply a sixth trophic 2004). Indeed, Southern sea lions have been identified
level for this ecosystem. as benthic and mid-water foragers along their Atlantic
The zooplankton community is dominated by Hum- range (Argentinean Patagonia), where the species is
boldt krill, the most abundant species in the Humboldt associated with a wide continental shelf that can reach
Current, with aggregations comparable to those of up to 400 km (Campagna et al., 2001; Thompson et al.,
Antarctic krill E. superba (Antezana, 2001, 2002). This 1998; Werner and Campagna, 1995). However, along
species appears to be an important prey for many pelagic the Pacific coast of South America the continental shelf
and demersal fishes and whales (Antezana, 1970). Our is considerably narrower or even absent, and therefore a
results confirm Humboldt krill as a primary consumer of divergence in the habits of sea lions can be expected
POM, especially considering the ability of krill to feed between the Atlantic and Pacific ranges. Our results
both at the surface and on the boundary of Oxygen suggest that Southern sea lions are epi- and mesopelagic
Minimum Layer below the main Humboldt Current, foragers along the Chilean coast, a strategy that is also
where POM is retained (Antezana, 2002). observed off Peru where sea lions prey predominantly
Trophic Position (TP) estimates can be obtained on anchovy (Soto et al., 2006).
using the dietary approach, based on the TP of prey It then becomes evident that conducting further
organisms and volumetric/gravimetric stomach content research on the trophic ecology and diving behavior of
data, or using the δ15N approach, based on the consistent Southern sea lions is necessary to obtain a better under-
isotopic enrichment of this element between prey and standing of their role as top predators in the ecosystem
predator (Vander Zanden et al., 1997). The pelagic and the different strategies utilized by the species in
132 L.A. Hückstädt et al. / Journal of Experimental Marine Biology and Ecology 347 (2007) 123–133

different ecosystems, as well as their interactions with S.A. (Eds.), Biology of Marine Mammals. Smithsonian Institution
fisheries. Press, Washington, pp. 423–484.
Bunn, S.E., Loneragan, N.R., Kempster, M.A., 1995. Effects of acid
washing on stable isotopes ratios of C and N in penaeid shrimp and
Acknowledgments seagrass: implications for food-web studies using multiple stable
isotopes. Limnology and Oceanography 40, 622–625.
We thank N. Llanos, E. Cisternas, S. Gacitúa, R. Mena, Burton, R.K., Koch, P.L., 1999. Isotopic tracking of foraging and long-
distance migration in northeastern Pacific pinnipeds. Oecologia
L.A. Cuevas, I. Municipalidad de Cobquecura, Pesca-
119, 578–585.
dores Artesanales Caleta Rinconada and Pesquera Itata Campagna, C., Werner, R., Karesh, W., Marin, M.R., Koontz, F.,
S. A. for their support during the sampling campaigns. R. Cook, R., Koontz, C., 2001. Movements and lactation at sea of
De Pol and O. Ulloa provided assistance with the isotopic South American sea lions (Otaria flavescens). Journal of Zoology
analyses. We also acknowledge M.C. Krautz and Labo- (London) 255, 205–220.
ratorio de Inmunología (Dpto. Bioquímica Clínica e In- Costa, D.P., Kuhn, C.E., Weise, M.J., Shaffer, S.A., Arnould, J.P.Y.,
2004. When does physiology limit the foraging behaviour of freely
munología, UdeC) for their help in processing the lipids. diving mammals? International Congress Series 1275, 359–366.
K. Yoda provided valuable assistance with the statistical Gannes, L.Z., O'Brien, D.M., Martínez del Río, C., 1997. Stable
analyses. S. Simmons, A-L Harrison and the Costa Lab at isotopes in animal ecology: assumptions, caveats, and a call for
UCSC provided useful comments on the manuscript. This more laboratory experiments. Ecology 78, 1271–1276.
study was funded by Grants in Aid or Research by Society George-Nascimento, M., Bustamante, R., Oyarzún, C., 1985. Feeding
ecology of the South American sea lion Otaria flavescens: food
of Marine Mammalogy (L.A.H), and Beca Jorge Tomicic contents and food selectivity. Marine Ecology Progress Series 21,
Karzulovic by Sociedad Chilenas de Ciencias del Mar — 135–143.
Minera Escondida Ltda. (L.A.H). This research was part Hall-Aspland, S.A., Hall, A.P., Rogers, T.L., 2005. A new approach to
of L.A.H's M.Sc. thesis (Departamento de Oceanografía, the solution of the linear mixing model for a single isotope:
UdeC), supported by Beca de Docencia (Escuela de application to the case of an opportunistic predator. Oecologia
(Berlin) 143, 143–147.
Graduados, UdeC). L.A.H's doctoral studies are sup- Hammill, M.O., Lesage, V., Carter, P., 2005. What do harp seals eat?
ported by the Fulbright-CONICYT (Chile) doctoral Comparing diet composition from different compartments of the
fellowships program. [MC] digestive tract with diets estimated from stable-isotope ratios.
Canadian Journal of Zoology 83, 1365–1372.
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