Small-scale variation in the diet of the South American Sea lion (Otaria flavescens) in northern Patagonia (Argentina)

Regional Studies in Marine Science 28 (2019) 100592

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Small-scale variation in the diet of the South American Sea lion (Otaria flavescens) in northern Patagonia (Argentina) ∗

Dayana Jarma a , María Alejandra Romero a,b,c , , Néstor A. García d , Guillermo Svendsen a,b,c , Raúl González a,b,c , Silvana Laura Dans d,e , Enrique Alberto Crespo d,e a

Centro de Investigación Aplicada y Transferencia Tecnológica en Recursos Marinos Almirante Storni, Güemes 1030 (8520) San Antonio Oeste (RN), Argentina b Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina c Escuela Superior de Ciencias Marinas, Universidad Nacional del Comahue, San Martín 247 (8520) San Antonio Oeste (RN), Argentina d Laboratorio de Mamíferos Marinos, Centro para el Estudio de Sistemas Marinos (CESIMAR) CENPAT- CONICET, Bvd. Brown 2915, 9120 Puerto Madryn, Chubut, Argentina e Universidad Nacional de la Patagonia San Juan Bosco, Bvd. Brown 3051, 9120 Puerto Madryn, Chubut, Argentina

article

info

Article history: Received 13 September 2018 Received in revised form 8 March 2019 Accepted 10 March 2019 Available online 13 March 2019 Keywords: Feeding habits Stomach content Variation in diet Sea lion

a b s t r a c t An understanding of the mechanisms that shape animal-population dynamics is a fundamental consideration in conservation biology and ecology. Populations of the species of South-American sea lions (SASLs) Otaria flavescens reveal different growth rates, which variations could be linked to changes in the accessibility of nutritional resources in any given location. The available information on differences in the SASL diet on a local scale, however, is relatively scarce. We therefore searched for evidence of geographical variations in the diet of the SASLs in Northern Patagonia—namely, in the Golfo San Matías (GSM) and the Golfo Nuevo (GN), both of which bays are quite different regarding their physiography, oceanography, and anthropic pressures. From 2005–2013, stomach samples ( nGSM = 39; nGN = 31) were collected from animals found dead on the coast or accidentally caught in fishing nets. The dietary composition differed between the two gulfs with respect to the most common species, the zoological groups, and the sizes of the primary prey. In the GSM, the SASLs fed on demersal–pelagic fish, while in the GN the diet exhibited a high contribution of benthic species. Differences in the items and sizes of prey consumed at each area are discussed in terms of differential prey availability along with the opportunistic feeding behavior of this predator. These differences, in addition to the species’s main prey as targets for major fisheries, must be taken into account in order to understand the different population dynamics of this apex predator and thus ensure its conservation. © 2019 Elsevier B.V. All rights reserved.

1. Introduction The habitat diversity of marine ecosystems can lead to a dependence on local niches that results in different population compositions for a single species—i.e., resulting from genetic differentiation and differences in resource exploitation (Valenzuela et al., 2009; Ohizumi and Miyazaki, 2010; Fernández et al., 2011). For instance, marine-mammal specialization in the use of local resources through individual choices in foraging behavior or diet promotes philopatry and leads progressively in the direction of genetic isolation (Hoelzel et al., 1998; Natoli et al., 2005; Chilvers and Wilkinson, 2009; Baylis et al., 2015b; Páez-Rosas et al., 2017; Rita et al., 2017). A comparison of the diets of a given species ∗ Correspondence to: Centro de Investigación Aplicada y Transferencia Tecnológica en Recursos Marinos Almirante Storni - CONICET, Güemes 1030 – (8520) San Antonio Oeste, Río Negro, Argentina. E-mail address: [email protected] (M.A. Romero). https://doi.org/10.1016/j.rsma.2019.100592 2352-4855/© 2019 Elsevier B.V. All rights reserved.

among diverse geographical regions and at different spatial scales is necessary to elucidate habitat use and population dynamics, as well as being crucial for assessing the trophic relationships of species of ecologic interest (Litvaitis, 2000), such as the South American Sea Lion (SASL) Otaria flavescens, the most conspicuous marine mammal along the South-American coasts. This apex predator was heavily exploited during the early 20th century for leather and oil (Videla, 1980; Crespo and Pedraza, 1991), and most of the populations were reduced to less than 10% of their original size (Crespo and Pedraza, 1991; Reyes et al., 1999; Romero et al., 2017). Today, the sizes of local populations are extremely dissimilar over the distribution range of the SASLs (Crespo et al., 2012). Certain populations are still decreasing (Venegas, 2001; Franco-Trecu, 2015), while others remain stable (Sepulveda et al., 2011) or otherwise are recovering at varying rates of increase (Dans et al., 2004; Grandi, 2010; De Oliveira et al., 2012; Baylis et al., 2015a; Romero et al., 2017). The circumstances responsible for this variability in the different patterns

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D. Jarma, M.A. Romero, N.A. García et al. / Regional Studies in Marine Science 28 (2019) 100592

of population dynamics are not understood with absolute certainty. In population ecology, however, one the most influential parameters determining population-growth rate is the relevant trophic ecology (Sibly et al., 2003). Certain authors have pointed out that the differing population tendencies observed among SASLs could be strongly linked to changes in the availability of feeding resources (Crespo et al., 2012). More recently, differences in foraging efficiency – involving diving physiology, dietary preferences, and prey distribution – over the distributional range of SASLs have been suggested as an additional mechanism to explain these contrasting population patterns (Hückstädt et al., 2016). Although studies have depicted the SASL as a generalist and opportunistic predator (Koen-Alonso et al., 2000; Romero et al., 2011; Muñoz et al., 2013), the information available on changes in the SASL’s dietary composition and feeding habits on a local scale is not abundant. Muñoz et al. (2013) found differences in the former parameter among populations in 3 geographic zones along the coast of Chile. Moreover, in the Falkland Islands (the Malvinas in Argentine terminology), the adult females manifested individual foraging specializations making use of both inshore and offshore habitats (Baylis et al., 2015b, 2016). The authors suggested that foraging specialization in depleted populations such as the SASLs breeding in the Falkland Island waters, was characterized by foraging-site fidelity and could thus be devoid of intraspecific competition (Baylis et al., 2015b). Information on habitat use and foraging behavior is therefore essential for a complete understanding of population dynamics and recoveries. In Northern Patagonia, the two most conspicuous gulfs – the Golfo San Matías and the Golfo Nuevo (Fig. 1) – are home to the majority of the SASL colonies of the region. The SASL population of Northern and Central Patagonia overall have been found to be recovering with a maximum increase rate of 0.055 (Romero et al., 2017), although at the local level the colonies from the Golfo San Matías exhibited a slightly higher instantaneous growth rate than those of the Golfo Nuevo—at respective values of 0.077 versus 0.058 between 1982 and 2008 (Grandi, 2010). These gulfs also differ greatly in their physiography, oceanography, and the associated anthropic pressures. The ecosystem of the Golfo San Matías is characterized by a high abundance of demersal and demersal–pelagic species, which are also exploited by industrial and artisanal fisheries (Romero et al., 2008). The demersal-fish community is dominated by the Argentine hake Merluccius hubbsi both in terms of biomass and fishery landings. More than 15 other fish species, however, have commercial and/or ecologic value, being mostly captured by trawlers as bycatch, but also being major prey resources for the SASLs (Romero et al., 2011). By contrast, no commercial fishing occurs in the Golfo Nuevo, though recreational fishing is prevalent, such as shore- and boatbased angling (Venerus and Cedrola, 2017) and spearfishing—that activity targeted mainly at mollusks (Ré, 1998a; Irigoyen and Venerus, 2008). This gulf is characterized by high water transparency, saturated oxygen conditions, and a bimodal optimization cycle of chlorophyll-a concentrations having maximum values in the autumn and spring and minimum values in the winter and summer, but nevertheless lower values than those registered in the Golfo San Matías. The limiting conditions for phytoplankton growth in the Golfo Nuevo would be the degree of sunlight in the winter and the water-column stratification year-round together with the nutrient levels in the summer (Williams et al., 2018). This gulf is impacted by both intensive tourist activities and effluents containing organic matter and heavy metals from the urban settlements in Puerto Madryn (Ferrando et al., 2010; Gil et al., 2014) and Puerto Pirámides. Studies of the fish communities in those two gulfs have pointed to a progressive replacement of subtropical components by temperate species in the north–south direction—i.e., from the Golfo San Matías to the Golfo Nuevo

(Galván, 2008; Jeres et al., 2018). The Golfo Nuevo also exhibited a higher abundance of certain components of the benthic community, such as the Patagonian red octopus, Enteroctopus megalocyathus, than the Golfo San Matías (Ré, 1998b; Ortiz et al., 2011). Those characteristics made these two areas a suitable setting to test a hypothesis concerning the differences in the diet of the SASLs on a local scale. Within this context, and taking to account the previous opportunistic feeding behaviors for this species, we hypothesized that the environmental differences between the Golfo San Matías and the Golfo Nuevo were relevant to the nature of the food supply for SASLs and that the species composition and sizes of the prey would differ considerably between those two areas. We expected that the SASL’s diet reflected the differential trophic availability in each of the gulfs, with a greater contribution of demersal– pelagic prey in the Golfo San Matías than that source in the Golfo Nuevo. Therefore, the aim of the present study was to conduct a comparative analysis of the diet and feeding habits of SASLs between the two gulfs with respect to prey composition, prey size, and feeding strategy. These data on the dietary comparison will, accordingly, provide a better understanding of the ecologic conditions that affect trophic ecology and the potential consequences with respect to the population dynamics of the SASLs in Patagonia. 2. Materials and methods 2.1. Analysis of stomach contents The determination of the composition of the diet of the SASL Otaria flavescens was based on an analysis of the stomach contents of 70 different individuals. Table 1 lists the 45 with stomach contents plus the 25 whose stomachs were empty. The subsample for the Golfo Nuevo was 31 stomachs from females (18) and males (13) found dead on the coast from 2005 to 2013. The subsample for the Golfo San Matías comprised 39 stomachs collected during the period from 2006 through 2012 from two sources: dead animals on the coast (26 specimens, 17 females and 9 males) and fishery bycatch (13 specimens). The bycatch specimens came from bottom trawlers targeting M. hubbsi (2 females, 9 males, and one of undetermined sex) and from pelagic net fishing for the Argentine anchovy Engraulis anchoita (1 male). Since the distance between the gulfs (150 km on average) is more than what either sex would travel in a day (Thompson et al., 1998; Campagna et al., 2001; Rodríguez et al., 2006; Baylis et al., 2015b, 2017), we assumed that the samples obtained from each study area were representative of each gulf and thus could be compared. In support of this assumption, the only study available involving satellite tracking of animals in the study area indicated that the sea lions from both gulfs did not overlap in their locations at sea during foraging trips (Campagna et al., 2001). The intact stomachs were removed and stored at −20 ◦ C in polyethylene bags. After thawing, the stomach contents were sorted through the use of sieves of different mesh sizes (from 0.5 to 10 mm). Although uncommon, intact prey were immediately identified, measured with Vernier calipers (±0.01 mm), and weighed with an electric balance (±0.01 g). Diagnostic hard parts (e.g., fish otoliths and bones, cephalopod beaks, and crustacean exoskeletons) were retrieved and stored in 70% (v/v) aqueous ethanol. The remains of prey were identified to the lowest possible taxonomic level according to the characteristics of the specimens in the reference collections of the Marine Mammals Laboratories (CENPAT-CONICET, Puerto Madryn and IBMPAS, San Antonio Oeste, Argentina) and in published catalogues (Clarke, 1986; Boschi et al., 1992; Gosztonyi and Kuba, 1996; Boltovskoy, 1999; Volpedo and Echeverría, 2000; García-Godos,

D. Jarma, M.A. Romero, N.A. García et al. / Regional Studies in Marine Science 28 (2019) 100592

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Fig. 1. Study area in Northern Patagonia and location of sampling sites (green dots). The geographic positions of the main rookeries of northern Patagonia are also showed (brown circles whose diameters reflect the number of individuals in each). Contours indicate different isobaths. Inset: the location of the study area within the Argentine Atlantic coastline. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.) Table 1 Sample of Otaria flavescens stomachs analyzed in the study according to geographical area, sex, age status, and source of sampling. Dead on shorea b

Area

GSM GN

c

Caught incidentally

Age status

Male

Female

Male

Female

Indeterminate

Adults Juveniles Adults Juveniles

3 (3) 3 4 (1) 5 (3)

8 3 4 2

5 5 0 0

1 1 0 0

1 0 0 0

(5) (1) (4) (7)

a

The number of empty stomachs is given in parentheses. GSM, Golfo San Matías; GN, Golfo Nuevo. c Females were considered mature at 4.8 ± 0.5 years old, corresponding to a mean standard body length (SL) of 147 cm; males between 4 and 6 years, or when they reach a mean SL of 212 cm (Grandi et al., 2010). b

2001). The total number of each fish consumed was determined from counts of left, right, and unassigned otoliths. The minimal number per species was obtained as the sum of half of the number of otoliths rounded off to the nearest whole number. The

number of cephalopods was estimated as the maximum number of upper or lower beaks (Pierce et al., 1991). In the example of crustaceans and annelids, the number of prey was determined from counts of cephalothorax, telsons, or clamps, and of upper

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or lower jaws, respectively. Complete and undigested elements (complete prey, otoliths, beaks, telsons, or cephalothoraxes) were measured with digital calipers. When digested or broken hard pieces were found in a stomach, the full measurements of these elements were assigned from a random sample of undigested and whole parts of the same species obtained within the same stomach (Koen-Alonso et al., 1998). The total length of fish (TL) and of the dorsal mantle (DML) of cephalopods (both in cm) and the wet weight (WW), in g, of the prey were estimated from the hard remains by means of allometric regressions (Pineda et al., 1996; Koen-Alonso et al., 2000). 2.2. Data analysis Intraspecific comparison of the diet of the SASLs between the Golfo San Matías and the Golfo Nuevo was based on the description of the dietary composition in each area by traditional indices. The prevalence of the different prey species in the diet was determined on the basis of the percent frequency of occurrence (%FO), the percentage by number (%N), the percentage by estimated wet weight (%W ) and the previously defined index of relative importance (%IRI; Pinkas et al., 1971; Cortés, 1997). The %FO was defined as 100 times the fraction of the stomachs in which a given prey species was present divided by the total number of stomachs with contents in the sample. The %N was calculated as 100 multiplied by the fraction of the number of individuals of a species of prey divided by the sum of individuals among all the prey species. The %W was obtained in a similar way as the %N but with the numbers being replaced by the weights estimated by regression (Hyslop, 1980). Finally, the IRI [IRIi = (%Ni + %Wi ) %FO] is a commonly used index that provides a summary of dietary composition (Koen-Alonso et al., 2000). In order to facilitate the interpretation of the IRI, this index was expressed as a percentage—i.e., %IRI (Cortés, 1997). These indices were calculated according to the species of prey, the major taxonomic groups (i.e., fish, mollusks, crustaceans, and annelids), and the ecologic groups—those being pelagic, benthic, and demersal. The last of these groups was divided into demersal–pelagic (with a daily vertical-migration pattern, thereafter dispersing in the water column during the night and remaining close to the bottom during early daylight hours) and demersal–benthic (no vertical migration occurring). To account for the uncertainty due to sampling, nonparametric 95% confidence intervals (95% CI) for %N and %W were generated by bootstrapping (Efron, 1979) by means of the software R (RCore Team, 2016). Random samples were drawn with replacement 1000 times. To examine the hypothesis that each prey was equally likely to be present in both gulfs, a test of homogeneity was performed by the Chi-square test. All prey with an %IRI greater than 1% in at least one sample were included in the analyses. Since the prey sizes consumed by a predator can also define differences in diet among subsets of individuals from the same species; the length-frequency distributions of the primary prey consumed were generated for both gulfs. The differences in prey sizes consumed were tested by using the nonparametric two-sample Mann–Whitney U test in those instances where differences were detected (Conover, 1980). The feeding strategy was assessed by the Costello graphical method (Costello, 1990) as modified by Amundsen et al. (1996). This calculation is based on a two-dimensional representation, where each point relates the frequency of occurrence of a given prey taxon, expressed as the percentage of stomachs in which that taxon is present (%FO) to its corresponding prey-specific abundance, defined as the percentage of occurrence of that prey

out of all of the prey items in the sum of only those stomachs in which that specific taxon appears (%P; Eq. (1)). %Pi = (Σi Si /Σti Sti ) × 100

(1)

Where Σi Si = the total of prey i (expressed as a number in this study), and Σti Sti = total of all the prey (expressed in number) in the stomachs with prey i. 3. Results The SASL body length ranged from 84 to 232 cm in the Golfo San Matías, and from 117 to 220 cm in the Golfo Nuevo. Of the 70 stomachs analyzed, 45 (Table 1) contained food remains (15 from the Golfo Nuevo, 30 from the Golfo San Matías; of which 45, 32 were from specimens dead on the coast, and 13 from bycatch). In general, the stomach contents were in an advanced state of digestion, being mostly composed of remaining hard parts (beaks, bones, and otoliths). From the Golfo San Matías samples, a total of 1102 prey were retrieved and 30 species identified; 19 of which were fish, 6 mollusks, and 5 crustaceans (Table 2). The mean (± SD) estimated biomass was of 4.1 ± 4.8 kg per stomach. The mean number of prey items per stomach was 36.7 ± 55.5. The mean number of individual prey per stomach was 57.6 ± 50.1 for the incidentally caught animals and 22.8 ± 55.9 for the stranded animals, but these differences were not statistically significant (F1,28 = 3.1, p = 0.08). From the Golfo Nuevo stomachs, 506 prey were counted and 27 species identified; 14 of which were fish, 6 mollusks, 5 crustaceans, and 2 polychaetes (Table 3). The total estimated biomass was 38.8 kg with a mean of 2.7 ± 2.5 kg per stomach. The mean number of individual prey per stomach was 33.7 ± 57.6. Neither the prey weights in kg nor the number of individual preys per stomach was statistically different between areas. 3.1. Dietary composition and relative prevalence of prey The dietary composition was specific for each gulf. In the Golfo San Matías, the three dominant species were fish: M. hubbsi (%IRI, 53.9%), the banded cusk-eel Raneya brasiliensis (%IRI, 14.8%), and the silver warehou Seriolella porosa (%IRI, 9.32), followed by Argentine short-fin squid Illex argentinus (%IRI, 5.95%). Another four species – the southwest-Atlantic butterfish Stromateus brasiliensis, the pink cusk-eel Genypterus blacodes, the Argentine anchovy Engraulis ancohita, and the Patagonian red octopus – presented %IRIs between 1 and 5% and as such were frequent prey items in the diet of the predator in that area (Table 2). In the Golfo Nuevo, the most frequent prey were the squid I. argentinus (%IRI, 33.5%) and the red octopus Enteroctopus megalocyathus (%IRI, 24.6%). Fish also represented major items in the sea lion diet there; the most abundant species being R. brasiliensis (%IRI, 11.8%), Genypterus blacodes (%IRI, 9.1%), and M. hubbsi (%IRI, 7.3%). Moreover, Doryteuthis gahi, Patagonotothen cornucola, Eledone massyae, and Octopus tehuelchus presented %IRIs ranging from 1 to 5% (Table 3). The results of the Chi-square test for homogeneity revealed 2 significant differences (X11 = 666.75; P < 0.001), indicating that the probability of prey in the diet did not consistently correspond to a sampling site. This discrepancy implies that the dietary composition of the SASLs differed between the two gulfs. Those differences remained when the analysis was carried out with only the specimens found dead on the coasts of both gulfs being 2 considered (X12 = 354.83; P < 0.001). The diet of the dead seals on the coast of the Golfo San Matías was characterized by a higher contribution of R. brasiliensis (%IRI, 63.7%) and I. argentinus (%IRI,

D. Jarma, M.A. Romero, N.A. García et al. / Regional Studies in Marine Science 28 (2019) 100592

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Table 2 Dietary composition of Otaria flavescens in the Golfo San Matías. Golfo San Matías Prey

Ecologic groupa

%FOb

%W

CI

%N

CI

%IRI

N

DP DB DP DP DB P B B DP B DB B B P B DB B D NA B B

38.71 25.81 19.35 16.13 19.35 12.90 19.35 3.23 6.45 9.68 3.23 6.45 3.23 3.23 6.45 3.23 3.23 3.23 9.68 3.23 3.23

34.94 4.64 20.77 11.69 8.68 1.81 0.39 0.96 1.27 0.52 0.09 0.54 0.64 0.22 0.23 0.14 0.31 0.25 – – –

15.55–55.83 0.16–16.39 5.20–40.75 0.45–30.05 2.27–21.44 0.02–6.64 0.10–0.92 0.00–4.32 0.00–4.32 0.00–1.58 0.00–0.42 0.00–1.49 0.00–2.45 0.00–0.85 0.00–0.91 0.00–0.59 0.00–1.17 0.00–0.94

37.11 24.95 4.17 3.54 2.00 9.89 1.72 2.63 0.45 0.45 2.18 0.36 0.54 0.82 0.27 0.27 0.09 0.09 0.09 0.09 0.09

14.25–65.82 1.54–53.93 1.22–12.81 0.35–12.31 0.54–5.75 0.37–26.29 0.60–3.74 0.00–10.45 0.00–1.81 0.00–1.40 0.00–8.65 0.00–1.25 0.00–2.25 0.00–2.25 0.00 −0.79 0.00–1.34 0.00–0.46 0.00–0.38 0.00–0.43 0.00–0.41 0.00–0.45

53.85 14.75 9.32 4.74 3.99 2.92 0.79 0.22 0.21 0.18 0.14 0.11 0.07 0.06 0.06 0.03 0.02 0.02 – – –

409 275 46 39 22 109 19 29 5 5 24 4 6 9 3 3 1 1 1 1 1

DP B DP B DP B

32.26 12.90 16.13 16.13 9.68 9.68

6.38 4.31 0.59 0.29 0.20 0.13

2.40–15.68 0.39–13.08 0.14–1.47 0.05–0.96 0.02–0.77 0.00–0.43

3.18 0.64 1.27 1.09 0.82 0.36

1.15–6.96 0.06–2.34 0.22–3.5 0.23–2.87 0.00–2.83 0.00–1.12

5.95 1.23 0.58 0.43 0.19 0.09

35 7 14 12 9 4

B B B DP B

6.45 3.23 3.23 3.23

0.00 0.00 – – 3.23

0.00–00

0.18 0.09 0.09 0.09

0.00–0.56 0.01

0.02

2 1 1 1 –

Fish Merluccius hubbsi Raneya brasiliensis Seriolella porosa Stromateus brasiliensis Genypterus blacodes Engraulis anchoita Porichthys porosissimus Triathalassothia argentina Macruronus magellanicus Paralichthys patagonicus Pinguipes brasilianus Xystreuris rasile Paralichthys isosceles Trachurus picturatus Prionotus nudigula Cynoscion guatucupa Psammobatis lentiginosa Callorhynchus callorhinchus Unidentified fish Ray egg Discopyge tschudii Mollusks Illex argentinus Enteroctopus megalocyathus Doryteuthis sanpaulensis Octopus tehuelchus Doryteuthis gahi Eledone massyae Crustaceans Tumidotheres maculatus Pterygosquilla armata armata Unidentified crab Eucopia sp. Rochinia gracilipes

–

– – 0.36

a

DP, demersal–pelagic; DB, demersal–benthic; P, pelagic; B, Benthic. %FO, percent frequency of occurrence; %N, percentage by number; %W , percentage by regression-estimated wet weight; %IRI, percent index of relative importance; N, number of prey items; CI, confidence intervals.

b

13.8%) than the corresponding values when the remainder of the dataset for this gulf were included (Table 2). In terms of ecologic groups (Fig. 2), the consumption patterns for the two gulfs were different. In the Golfo San Matías the demersal–pelagic prey was the most highly represented group; followed by the demersal–benthic, the benthic, and finally the pelagic prey; whereas in the Golfo Nuevo the diet contained a high contribution of benthic prey, which group ranked second in the following order of prevalence: demersal–pelagic, benthic, demersal–benthic, and pelagic. Moreover, the distribution of prey among the different ecologic groups was more uniform in the Golfo Nuevo than in the Golfo San Matías. Furthermore, differences in zoological groups (Fig. 3) were also found between the two gulfs; with the main group consumed by the sea lions in the Golfo San Matias being fish (%IRI, 91.3%), but in the Golfo Nuevo cephalopods (%IRI, 58.3%). Differences between the sexes were explored only qualitatively because the number of samples with respect to sex, gulf, and sample origin prevented a quantitative analysis. Among only the samples from the animals found dead on coasts of the two gulfs, sex-specific dietary differences were found. In the Golfo Nuevo, the males preyed on I. argentinus (%IRI, 52.4%), E. megalocyathus (%IRI, 13.0%), Doryteuthis gahi (%IRI, 10.6%), and G. blacodes (%IRI, 10.5%); while the females fed on E. megalocyathus (%IRI, 30.2%), R. brasiliensis (%IRI, 37.3%), and M. hubbsi (%IRI, 17.4%). In Golfo San Matías, the males preyed on R. brasiliensis (%IRI, 82.6%) and I. argentinus (%IRI, 7.19%); while the females

Fig. 2. Dietary composition of the South-American sea lion Otaria flavescens in the Golfo Nuevo (GN, gray bars) and the Golfo San Matías (GSM, black bars) with respect to the ecologic groups of prey (mean and error bars). %IRI, percent index of relative importance; DP, demersal–pelagic; DB, demersal–benthic; B, benthic; P, pelagic. In the figure the %IRI is plotted on the ordinate for each of the ecologic groups indicated on the abscissa. The error bars are the nonparametric 95% confidence intervals (95% CI) generated by bootstrapping.

fed on G. blacodes (%IRI, 24.7%), Triathalassothia argentina (%IRI, 16.2%), I. argentinus (%IRI, 13.9%), and Pinguipes brasilianus (%IRI, 9.73%).

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Table 3 Dietary composition of Otaria flavescens in Golfo Nuevo. Golfo Nuevo Prey

Ecologic groupa

%FOb

%W

CI

%N

CI

%IRI

N

DB DB DP DB B P B P B B B DB NA

26.67 26.67 33.33 26.67 13.33 6.67 6.67 20.00 6.67 6.67 6.67 6.67 13.33

5.49 19.91 7.68 0.43 0.05 0.15 0.11 0.22 0.03 0.02 0.00 – –

0.11–18.19 0.41–53.44 1.64–18.91 0.02–1.11 0.00–0.15 0.00–0.75 0.00–0.38 0.00–0.88 0.00–0.10 0.00–0.05 0.00–0.00 – –

22.53 1.78 6.13 8.89 0.79 0.40 0.20 0.99 0.20 0.20 0.20 0.20 0.40

1.85–51.08 0.25–7.24 0.75–12.55 0.42–35.04 0.00–3.48 0.00–2.08 0.00–0.49 0.00–5.21 0.00–0.49 0.00–0.49 0.00–1.04 0.00–1.04 0.00–1.63

11.77 9.11 7.25 3.92 0.18 0.06 0.03 0.38 0.02 0.02 0.02 – –

114 9 31 45 4 2 1 5 1 1 1 1 2

DP B DP B B DP DP

40.00 40.00 20.00 26.67 20.00 6.67 6.67

22.30 37.67 2.65 1.57 0.93 0.17 –

2.66–54.07 11.63–75.40 0.05–9.53 0.20–4.43 0.08–2.92 0.05–9.53 –

30.83 1.38 11.26 4.35 4.35 1.58 0.20

2.00–62.13 0.37–4.62 0.00–22.48 0.45–9.06 0.00–19.77 0.00–3.93 0.00–22.48

33.48 24.61 4.38 2.48 1.66 0.18 –

156 7 57 22 22 8 1

B B B B B B

6.67 6.67 6.67 6.67 6.67 6.67

0.46 0.06 0.04 0.02 0.02 –

0.00–1.65 0.00–0.27 0.00–0.16 0.00–0.08 0.00–0.07 –

0.40 0.20 0.20 0.20 0.20 0.20

0.00–2.57 0.00–1.27 0.00–1.25 0.00–1.04 0.00–0.49 0.00–1.25

0.09 0.03 0.02 0.02 0.02 –

2 1 1 1 1 1

B B

13.33 6.67

0.03 –

0.00–0.09 –

1.19 0.20

0.00–7.08 0.00–1.04

0.25 –

6 1

Fish Raneya brasiliensis Genypterus blacodes Merluccius hubbsi Patagonotothen cornucola Bovichthys argentinus Trachurus picturatus Paralichthys isosceles Engraulis anchoita Triathalassothia argentina Agonopsis chiloensis Xystreuris rasile Percophis brasiliensis Unidentified fish Mollusks Illex argentinus Enteroctopus megalocyathus Doryteuthis gahi Eledone massyae Octopus tehuelchus Doryteuthis sanpaulensis Doryteuthis spp. Crustaceans Ovalipes trimaculatus Peltarion spinosulum Pterygosquilla armata armata Libinia spinosa Munida sp. Unidentified crab Anellids Eunice argentinensis Aphroditidae a

DP, demersal–pelagic; DB, demersal–benthic; P, pelagic; B, Benthic. %FO, percent frequency of occurrence; %N, percentage by number; %W , percentage by regression-estimated wet weight; %IRI, percent index of relative importance; N, number of prey items; CI, confidence intervals.

b

Fig. 3. Dietary composition of the South-American sea lion Otaria flavescens in the Golfo Nuevo (GN, gray bars) and the Golfo San Matías (GSM, black bars) with respect to the zoological groups of prey (mean and error bars). %IRI, percent index of relative importance. In the figure the %IRI is plotted on the ordinate for each of the zoologic groups indicated on the abscissa. The error bars are the nonparametric 95% confidence intervals (95% CI) generated by bootstrapping.

3.2. Analysis of prey size The overall estimated length of prey consumed ranged from 1.7 to 90.9 cm, while the estimated weight range was 0.04– 6720 g. Of the prey eaten by the sea lions, 90% was concentrated in classes ranging between 7.7 and 37.4 cm. The smallest prey were the pelagic crustaceans (Munida gregaria) and the

cephalopods (Doryteuthis sanpaulensis), whereas the upper end of the length-distribution data represented fish such as Bovichthys argentinus and G. blacodes. The sea lions from the Golfo San Matías preyed on significantly larger-sized prey than those of the GolfoNuevo specimens (GSM = 20.4 ± 9.45 cm, GN = 14.1 ± 10.5 cm; U = 203, 404.50; P < 0.001). With respect to the species of prey, the Argentine short-fin squid (Fig. 4, Panel A) evidenced a unimodal length-frequency distribution with a mean length of 17.9 ± 8.7 cm (range: 5.1– 39.1) in the Golfo San Matías and 11.4 ± 5.3 (range: 4.4–30.1 cm) in the Golfo Nuevo. Most of sea lions from the Golfo Nuevo consumed squids smaller than 15 cm, while in the Golfo San Matías the prey were larger individuals. According to size, the individuals consumed in the Golfo San Matías were both juvenile and mature, while those prey from the Golfo Nuevo were only juvenile (Crespi-Abril et al., 2008, 2010a). Significant differences were found in the sizes of the M. hubbsi (U = 8212.50; P < 0.05) and the I. argentinus (U = 5116.50; P < 0.001) consumed by the sea lions between the two gulfs. The M. hubbsi consumed by the sea lions (Fig. 4, Panel B) had a mean length of 23.0 ± 7.7 cm (range: 6.9–49.2) in the Golfo San Matías and one of 24.6 ± 4.9 cm (range: 11.5–32.5) in the Golfo Nuevo; with the length-frequency distribution being unimodal in both gulfs. Of the M. hubbsi consumed by this predator, 75% were under 30 cm of length, with such a size corresponding to juvenile individuals (Ocampo-Reinaldo, 2010).

D. Jarma, M.A. Romero, N.A. García et al. / Regional Studies in Marine Science 28 (2019) 100592

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Fig. 4. Box plots of the dorsal mantle length (DML) of the squids Illex argentinus (Panel A) and the total length (TL) of the hakes Merluccius hubbsi (Panel B) consumed by the South-American sea lion Otaria flavescens in the Golfo San Matías (GSM) and the Golfo Nuevo (GN). In the box plots, the DML (Panel A) or the TL (Panel B) is plotted on the ordinate for individuals from each of the gulfs indicated on the abscissa, where the upper and lower borders represent the quartiles of the data, the square the median, the upper and lower brackets (the whiskers) the maximum and minimum values, and the dots the outriders (inset to the right).

Fig. 5. Amundsen diagrams illustrating the feeding strategy of the South-American sea lion Otaria flavescens in the Golfo San Matías (GSM, Panel A) and the Golfo Nuevo (GN, Panel B). The percentage (expressed as numbers) of the indicated prey present among the total prey items in the stomachs of all those prey-specific predators (%Pi ) is plotted on the ordinate as a function of the percentage of total predator stomachs in which that prey item occurred (%FO) on the abscissa. The interpretation of Amundsen’s diagram can be obtained by examining the distribution of points along the diagonals and axes of the graph. The diagonal from the lower left to the upper right corner provides a measure of the frequency of prey prevalence among all the predators with the dominant prey plotting at the upper right and the rare or inconsequential prey at the lower left. The ordinate represents the feeding strategy of the predator in terms of specialization or generalization. In general, predators specialize in prey positioned in the upper part of the graph, but eat those positioned in the lower part only occasionally. The prey points located at the upper left of the diagram are indicative of specialization by individual predators, whereas those loci in the upper right represent specialization by the whole population of predators.

3.3. Feeding strategy For both gulfs, the analysis of the feeding strategy based on the Amundsen graphical method indicated that SASLs exhibited a generalist feeding pattern. Most of the prey were consumed at a low frequency and a low abundance (Fig. 5). Prey species with a low frequency of occurrence and a low prey-specific abundance by number (%N) located in the lower left corner were considered complementary food items. Cynoscion guatucupa in the Golfo San Matías and Callorhynchus callorinchus in the Golfo Nuevo represent examples of specialization at individual level, with those prey being consumed by few individuals (low %FO), but with high prey-specific abundance (%P). Also notable in the figure is the difference in the nature and distribution of the three most frequent and prevalent points between the two gulfs—i.e., C. guatucupa, M. hubbsi, and R. brasiliensis (Panel A) and C. callorhinchus, R. brasiliensis, and I. argentinus (Panel B)—that further illustrates the

discrepancy in the dietary patterns of the sea lions inhabiting the two separate areas. 4. Discussion Except for a single study comparing the qualitative and quantitative nature of the diet in females through the use of isotopes (Drago et al., 2011); the present work constitutes the first attempt at quantifying and comparing the diet and feeding strategy of the SASLs in the sea off north Patagonia on a local scale. The main aim of that study, however, was to evaluate the growth of pups and not to compare the diets between locations. Thus, the authors, making such comparisons as an ancilla to the principal study, found no differences in the dietary composition of individuals between two colonies that were separated from each other by only ca. 3 kilometers.

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In contrast, previous studies for other pinniped species based on stomach contents had pointed to local geographical differences in the diet (Bowen et al., 1993; Tollit et al., 1998; Casaux et al., 2003; Baylis et al., 2016) and reported that the largest portion of the observed variation in the diet was attributable to the geographic region and to the prey availability (Lundström et al., 2010). Nevertheless, other parameters such as age, sex, and season may contribute to the dietary composition to a lesser extent (Lundström et al., 2010). Although these variables were not numerically evaluated in the present study, we did find differences between the sexes. Similar results had been previously cited for north and central Patagonia, where the females were found to feed on mostly benthic species, whereas the males fed on mainly demersal–pelagic prey (Koen-Alonso et al., 2000). Future analyses need to be performed to continue exploring the source of that variability. In each of the two gulfs, the predator exhibited a different pattern of prey-resource exploitation within the various ecologic groups. For instance, in the Golfo Nuevo the SASLs preyed mainly on food associated with the bottom (57.7% corresponding to the benthic and the demersal–benthic fauna), as such departing from the demersal–pelagic foraging observed in Golfo San Matías (in 70.7% of the diet). In this latter gulf, fish mainly dominated the diet (91.3%). This result agrees with previous dietary studies that depicted SASLs as essentially a piscivorous predator (Thompson et al., 1998; Koen-Alonso et al., 2000; Suarez et al., 2005; Romero et al., 2011; Bustos et al., 2012; Machado et al., 2018). In addition, the high contribution of benthic prey in the Golfo Nuevo could be associated with changes in the structure of reefs in that area, since the invasion of the macro alga Undaria pinnatifida has reduced the abundance of the fish (Irigoyen et al., 2011) at the same time as simultaneously increasing the species diversity in the benthic macrofauna (Irigoyen and Galván, 2010). Over the distribution range of SASLs, we found evidence of both types of resource exploitation. Studies on dietary data have suggested that SASLs forage in the epipelagic zone throughout their range in the Pacific (Hückstädt and Krautz, 2004; Soto et al., 2006; Hückstädt et al., 2007, 2014). In Uruguay, Riet-Sapriza et al. (2013) found that lactating SASLs are benthic divers and forage in shallow water within the continental shelf. The demersal and benthic prey had also a greater prevalence than other ecologic groups in the diet of the SASLs from the Brazilian coast (Machado et al., 2018). Of particular relevance among our findings is that two of the main prey found in the Golfo-San-Matías samples, the hake M. hubbsi and silver warehou S. porosa, are also the main demersal fishery resources of the area (Ocampo-Reinaldo, 2010; Romero et al., 2008). Of those two, the more highly exploited and economically relevant is M. hubbsi, it being fished mainly by a trawl demersal fleet (Romero et al., 2010). The high contribution of M. hubbsi to the diet of sea lions in the Golfo San Matías may result from two circumstances. First, this fish species is highly available in the environment as part of an independent stock of hake within the Golfo San Matías (Sardella and Timi, 2004; González et al., 2007; Machado-Schiaffino et al., 2011) with a population structure that seems to have been stable since the beginning of the fishery in 1970 (González et al., 2007; OcampoReinaldo, 2010). Second, the catching and discarding of M. hubbsi by trawl nets and artisanal midwater longlines quite certainly increases the accessibility of this prey to the predator; indeed the stomachs with the more frequent occurrence of M. hubbsi have come precisely from animals caught incidentally while in the act of predation on net catches. The commercial fishery discards about 2000 metric tons of undersized (<30 cm) hake annually (Romero et al., 2010), and those discarded fish have been hypothesized as producing a major availability of the hake for sea lions (Drago et al., 2009). This fraction of hakes smaller than 30 cm

is, furthermore, precisely the length targeted by sea lions. Over the distribution range of the SASLs, the presence of individuals preying on fishery catches has been widely reported (Hückstädt and Antezana, 2003; Szteren et al., 2004). In the Golfo San Matías, operational interactions between SASLs and trawlers (Romero et al., 2017) plus long-line fleets (González-Zevallos and Firstater, 2004) have been reported. Campagna et al. (2001) also found that the feeding zones of SASLs and the fishing areas in Golfo San Matías overlap. From an ecologic perspective, the existence of a low general trophic overlap between trawler fishing and the SASLs within the gulf has been suggested (Romero et al., 2011), but the strongest overlap was found to be with respect to the specific consumption of small hake. The silver warehou is a seasonal demersal resource within the Golfo San Matías that is fished from August to October (Perier and Di Giácomo, 2002; Romero et al., 2008). In the present study, the sea lions that preyed on this species did so during periods when the catches reached the maximum landings, indicating that during this period of greatest abundance, both the sea lions and the fishing fleet exploited this resource. This observation, coupled with the dominance of the silver warehou in the diet of sea lions from Golfo San Matías and the total absence of that species in Golfo Nuevo stomach samples, further underscores the opportunistic feeding behavior of SASLs in northern Patagonia. Inferences on foraging habits through the interpretation of dietary results are often limited by the inherent biases present in any method of diet analysis (e.g., Da Silva and Neilson, 1985; Jobling and Breiby, 1986; Meynier et al., 2008. Sea lions found dead on shore may include animals that were sick and had not fed normally immediately before dying. Bycaught animals, furthermore may have stomach contents biased towards the particular target species of the fishery. Notwithstanding, in our sample the stranded individuals contained a high number of prey items, and the differences in the diet were still found when the comparison was carried out when only the samples from animals found dead on the coast were considered. Furthermore, feeding on fishery catches represents an alternative source of food for the populations of the Golfo San Matías in contrast to the circumstance in the Golfo Nuevo, and therefore those individuals that were caught in nets were deliberately included for the completeness of the analysis. The high contribution of the red octopus E. megalocyathus in the diet of the Golfo Nuevo individuals agrees with previous studies. Koen-Alonso et al. (2000) identified this species as the main prey for the females of the SASLs in samples from northern and central Patagonia. That study, however, did not analyze changes in the dietary composition on the local scale, and therefore the report summarizes the feeding habits for a broad area. The high contribution of E. megalocyathus in the GolfoNuevo samples agrees with the high availability of this prey in that area. The red octopus lives on hard benthos – mainly within the intertidal zone, but even up to 140 m of depth – and has been described as a common species from rocky reefs in the Golfo Nuevo (Ré, 1998b; Ortiz et al., 2011). In contrast, in the Golfo San Matías the abundance of that species is significantly lower since that region represents the northernmost limit of its distribution range. With respect to I. argentinus, the main prey for the SASL in the Golfo Nuevo, no data are available on that squid’s abundance in this gulf, though the proposal has been raised that this area represents a nursery zone (Crespi-Abril et al., 2010b). R. brasiliensis was another prey making a high contribution to the diet in both gulfs, with previous studies having also reported the presence of this item in the SASL diet (Koen-Alonso et al., 2000; Suarez et al., 2005; Romero et al., 2011; Bustos et al., 2012). Unfortunately, little is known about the ecology of this fish—even

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though R. brasiliensis constitutes a key link in the food web of the south Atlantic Ocean and is a major prey item in the diet of marine mammals, marine birds, and fish (Malacalza et al., 1994; Koen-Alonso et al., 2000, 2001, 2002). As to the prey sizes consumed, in both gulfs the sea lions preyed mainly on juvenile classes of M. hubbsi. Particularly in Golfo San Matías, the length-frequency distribution of the hake consumed and that of the hake resource overlapped considerably (Ocampo-Reinaldo, 2010; Romero et al., 2011). This observation also suggests an opportunistic feeding behavior of the predator. Unfortunately, no information about the length frequency distribution of hake in the Golfo Nuevo is available. In the case of Argentine short-fin squid, the SASLs from the Golfo San Matías preyed on bigger sizes and over a wider range than the individuals from the Golfo Nuevo. This finding agrees with size availability; this species feeds, reproduces, and spawns in the Golfo San Matías, and two cohorts of squids are present there: the first characterized by larger individuals (20–35 cm) and the second by smaller ones (14–25 cm; (Crespi-Abril et al., 2010a); whereas in Golfo Nuevo the presence of only paralarvae (1.2 to 6.5 cm) and juveniles (5 to 6.5 cm) has been reported, very likely because that gulf is exclusively a nursery area (Crespi-Abril et al., 2010b). The Amundsen diagrams in Fig. 5 pointed to a generalist strategy in the diet of the SASLs of both northern Patagonian gulfs. This analysis, together with the diversity of the prey species recorded and the ecologic and zoologic groups consumed, confirmed that the SASL is a broad-spectrum predator (Koen-Alonso et al., 2000; Romero et al., 2011; Bustos, 2013). In addition, the differential consumption of different prey and sizes – those being often associated with resource availability within the environment and constituting mainly species for which data on abundance and distribution size are available – indicated that the SASL is likewise an opportunistic predator. From the standpoint of conservation, the differences observed on the small-scale level should be taken into account in studies of population dynamics in the region. In Patagonia, benthic species are the lowest in lipid content and consequently had the lowest energetic values, while demersal–pelagic fish are higher in lipid and caloric content (Eder and Lewis, 2005). Furthermore, the pups of SASL females that mostly rely on offshore pelagic prey grow faster than those of females that base their diet on coastal benthic items (Drago et al., 2010). Thus, the type of prey and the corresponding energetic intake could contribute, among other parameters, to the higher population rates of the SASLs in the Golfo San Matías: indeed, the diet of those individuals consists of a larger percentage of demersal and pelagic prey than the diets in the Golfo Nuevo, together with other relevant prey – such as S. porosa and S. brasiliensis – that are exclusively present in that gulf, both of which species represent very high energetic values. 5. Conclusions Our results have demonstrated that the diet of the SASL O. flavescens differs between the Golfo San Matías and the Golfo Nuevo; in particular with respect to the dominant species, the ecologic and zoologic groups, and the sizes of the prey consumed. This finding indicates a high flexibility in the predator’s diet, and also underscores the value of local-scale studies in enabling a complete characterization of the diet and an understanding of different population contexts over the overall distribution range of this species. In northern and central Patagonia, where the population is recovering after a depletive harvest and the fishery is expanding its operational range, the acquisition of detailed data on the trophic ecology of the SASL represents an essential input for the construction of food-web models that are presently

9

severely limited by the quality of the available data. Thus, a development of models within a scale-based framework that explicitly consider small-scale variations in the diet of predators would allow the creation of management and conservation objectives on a more comprehensive and realistic basis. Acknowledgments We are indebted to many people from the Marine Mammal Laboratory at the Centro Nacional Patagónico (Puerto Madryn, Argentina) and the Institute of Marine Biology and Fisheries (San Antonio Oeste, Argentina) for their assistance in the field work during the last 40 years. This study was carried out with logistical support by the Centro Nacional Patagónico (CONICET) and the Instituto de Biología Marina y Pesquera Alte. Storni. The funding was based on long-term field work supported by Amnéville Zoo, France (2005–2015), BBVA Foundation (BBVA, BIOCON 04) (2005–2008), ANPCYT (PICT 33934, PICT 2110, PICT 2014–1671) (2007–2015), Yaqu-pacha, Heidelberg Zoo.(2012) and The Mohamed Bin Zayed Species Conservation Fund. (2011– 2014). Dr. Donald F. Haggerty, a retired academic career investigator and native English speaker, edited the final version of the manuscript. Declarations of interest None. References Amundsen, P.A., Gabler, H.M., Staldvik, F.J., 1996. A new approach to graphical analysis of feeding strategy from stomach contents data—modification of the Costello (1990) method. J. Fish. Biol. 48, 607–614. Baylis, A.M.M., Kowalski, G.J., Voigt, C.C., Orben, R.A., Trillmich, F., Staniland, I.J., Hoffman, J.I., 2016. Pup vibrissae stable isotopes reveal geographic differences in adult female southern sea lion habitat use during gestation. PLoS One 11, 1–11. Baylis, A.M.M., Orben, R.A., Arnould, J.P.Y., Christiansen, F., Hays, G.C., Staniland, I.J., 2015a. Disentangling the cause of a catastrophic population decline in a large marine mammal. Ecology 96, 2834–2847. Baylis, A.M.M., Orben, R.A., Arnould, J.P.Y., Peters, K., Knox, T., Costa, D.P., Staniland, I.J., 2015b. Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion. Oecologia 179 (4), 1053–1065. Baylis, A.M., Orben, R.A., Costa, D.P., Tierney, M., Brickle, P., Staniland, I.J., 2017. Habitat use and spatial fidelity of male South American sea lions during the nonbreeding period. Ecol. Evol. 7 (11), 3992–4002. Boltovskoy, D., 1999. South Atlantic Zooplankton. Backhuys Publishers, Leiden. Boschi, E.E., Fischbach, C.E., Iorio, M.I., 1992. Catálogo ilustrado de los crustáceos estomatópodos y decápodos marinos de Argentina. Frente Marítimo, Mar del Plata. Bowen, W.D., Lawson, J.W., Beck, B., 1993. Seasonal and geographic variation in the species composition and size of prey consumed by grey seals (Halichoerus grypus) on the Scotian Shelf. Can. J. Fish. Aquat. Sci. 50, 1768–1778. Bustos, R.L., 2013. Variación espacio-temporal en la dieta de Otaria flavescens (Carnivora: Otariidae) en las costas de Río Negro (Ph.D. dissertation). Universidad Nacional de Córdoba Córdoba, Argentina. Bustos, R.L., Daneri, G.A., Volpedo, A.V., Harrington, A., Varela, A.E., 2012. The diet of the South American sea lion (Otaria flavescens) at Río Negro, Patagonia, Argentina, during the winter-spring period. Iheringia Sér Zool 102, 394–400. Campagna, C., Werner, R., Karesh, W., Marín, M.R., Koontz, F., Cook, R., Koontz, C., 2001. Movements and location at sea of South American sea lions (Otaria flavescens). J. Zool. 255, 205–220. Casaux, R., Baroni, A., Arrighetti, F., Ramón, A., Carlini, A., 2003. Geographical variation in the diet of the Antarctic fur seal Arctocephalus gazelle. Polar. Biol. 26, 753–758. Chilvers, B.L., Wilkinson, I.S., 2009. Diverse foraging strategies in lactating New Zealand sea lions. Mar. Ecol. Prog. Ser. 378, 299–308. Clarke, M.R., 1986. Cephalopods in the diet of odontocetes. In: Bryden, M.M., Harrison, R. (Eds.), Research on Dolphins. Oxford University Press, Oxford. Conover, W.J., 1980. Practical Nonparametric Statistics, 3rd edition. John Wiley & Sons, New York. Cortés, E., 1997. A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Can. J. Fish. Aquat. Sci. 54, 726–738.

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