Marine Biology

, 165:86 | Cite as

Diversification of foraging habits among Guadalupe fur seals from their only well-established breeding colony, Guadalupe Island, Mexico

  • Ariadna Juárez-Ruiz
  • Fernando R. Elorriaga-Verplancken
  • Xchel G. Moreno-Sánchez
  • Sergio Aguíniga-García
  • María José Amador-Capitanachi
  • Casandra Gálvez
Original paper


Intra-population resource partitioning is a foraging strategy that could minimize intra-specific competition. This behavior may be ecologically relevant for species in recovery like the Guadalupe fur seal Arctocephalus philippii townsendi (GFS), which was considered extinct 70–80 years ago. The present study provides, via scat and stable isotope (δ15N and δ13C) analyses, trophic knowledge around GFSs from Guadalupe Island just prior to and the 2013 breeding season, with emphasis on inter-individual variability. A total of 107 scat samples were analyzed, and 98 neonate fur samples (proxies for adult female foraging) were isotopically assessed. The overall trophic spectrum included 12 items, with a slight increase in diversity among main prey during the second half of the breeding season. The isotopic analysis revealed three distinct groups, reflecting apparent variations in trophic position and coastal/oceanic habitat use. As in previous studies, a mostly teutophagous diet was clear; however, our work is the first to identify inter-individual prey and habitat partitioning. Based on our results and those of other studies, GFSs exhibited an opportunistic foraging strategy across the breeding season. Both analyses were complementary in terms of diversification and useful for the understanding GFS foraging strategies, which are relevant to evaluating population recovery as factors such as prey availability is suggested to be critical to this species recovery.


Dietary studies have been paramount in establishing the role of pinnipeds within the trophic web, improving our understanding of predator–prey relationships, elucidating interactions with fisheries due to pinniped consumption of commercially important prey resources, and revealing changes (e.g., prey availability) in the ecosystem they inhabit (Arim and Naya 2003; Casper et al. 2006; McClatchie et al. 2016). Among the foraging displays by pinnipeds and other predators, researchers have observed the differential use or partitioning of resources in terms of both the habitats exploited and the prey consumed. This population behavior may reduce intra-species competition through the formation of groups with different foraging specializations (Bolnick et al. 2003; Vander Zanden et al. 2010). Identifying this behavior, particularly in a species in recovery, is of the utmost importance to improve our ecological understanding of their re-establishment and to propose conservation programs for these species and their habitats. One such species is the Guadalupe fur seal (GFS) Arctocephalus philippii townsendi, which is classified as an endangered species under Mexican law NOM-059-ECOL-2010 (SEMARNAT 2010). Currently, this species is distributed on Guadalupe Island, which is the species’ only well-established breeding colony. It can also be found on the San Benito Archipelago, which is a recolonization site with rare presence of births (Elorriaga-Verplancken et al. 2016a), and in limited numbers on the islands off the coast of California, USA, including San Miguel and the Farallon Islands (Gallo-Reynoso 1994; Hanni et al. 1997; Aurioles-Gamboa et al. 2010). The abundance of GFSs is estimated to be approximately 17,500 for Guadalupe Island (García-Capitanachi et al. 2017) and around 2600 (3700 in 2014 and 1500 in 2015) for San Benito (Elorriaga-Verplancken et al. 2016a). This species exhibits a polygynous reproductive strategy with breeding occurring during summer (June–August) when each adult female gives birth to one pup. Lactation lasts 8–9 months (Gallo-Reynoso 1994), during which time females alternate between nursing their pups and undertaking long foraging trips lasting up to (mean ± SD) 14.4 ± 8.3 days and covering distances of 444 ± 151 km each (Gallo-Reynoso et al. 2008).

Available GFS dietary data derived from studies carried out on Guadalupe Island (Gallo-Reynoso 1994; Hernández 2009), the Farallon Islands (Hanni et al. 1997), and the San Benito Archipelago (Aurioles-Gamboa and Camacho-Ríos 2007; Pablo 2009; Esperón Rodriguez and Gallo-Reynoso 2012; Amador-Capitanachi et al. 2017), in which eight squid species have been identified, especially opalescent squid Doryteuthis opalescens and hooked squid Onychoteuthis banksii, which have stood out as the main prey for GFSs from these three locations. However, some of this information is based on small sample sizes (e.g., 5 scats or unknown sizes), with cephalopod beaks, fish otoliths, and other prey remnants being identified in scat and regurgitated matter. This methodology (scat analysis) has traditionally been used to describe dietary composition (Casper et al. 2006). This approximation assumes that the hard structures in a scat are encountered in the same proportions in which they were consumed during the individual’s last foraging event (Tollit et al. 1997). This technique is highly useful but it may present bias due to the accumulation (Pierce and Boyle 1991) or degradation of hard structures (da Silva and Neilson 1985, Tollit et al. 1997). Therefore, a powerful approach is to combine techniques, including others such as the analysis of stable isotopes of carbon (δ13C) and nitrogen (δ15N) (Orr et al. 2011). Values of δ13C allow us to infer habitat use and the corresponding carbon sources, while δ15N reflects the trophic position and breadth (Newsome et al. 2007). The δ13C and δ15N values originate in the base of the trophic web and both present constant and relatively predictable enrichment or trophic discrimination factor (0.5–1.0 and 3–5 ‰, respectively) from the base to the upper levels; thus, apex predators are an efficient indicator of the variations in the trophic web. One of the advantages of this method is the broad temporal window that can be assessed depending on the type of tissue analyzed and its specific turnover or growth rate (Minagawa and Wada 1984; Hobson and Welch 1992).

Several studies on the trophic ecology of pinnipeds have used neonates as proxies for their mothers when conducting stable isotope analysis (e.g., Porras-Peters et al. 2008; Páez-Rosas and Aurioles-Gamboa et al. 2010). Neonates fur (lanugo), such as the one used for our study, was formed by maternal catabolism during the last ~ 12 weeks of gestation and ~ 4 weeks of lactation, when fur continues to grow (personal observation by authors on neonates marked with furcuts for a parallel study), creating a trophic relationship between pup and mother that is similar to that between predator and prey (Habran et al. 2010; Elorriaga-Verplancken et al. 2016b). Hence, the fur of GFS neonates has a higher δ15N value (~ 1‰) but shows almost no difference in δ13C (~ − 0.2‰) relative to their mothers (Elorriaga-Verplancken et al. 2016b). Because of these consistent differences, the variation between groups of neonates is attributed to differences in their mothers’ foraging habits.

The goal of the current study was to provide novel information by simultaneously employing complementary techniques (scat and stable isotope analyses) to assess the foraging habits of GFSs at their only well-established breeding site (Guadalupe Island) at two different temporal scales. Our study focuses on prey and habitat partitioning, ecological aspects that are important for better understanding changes in this species’ population distribution and abundance.

Materials and methods

Samples for the scat and stable isotope analyses were collected during the 2013 breeding season (June to August) at three sites on Guadalupe Island: Las Casitas, Corralitos, and Punta Sur (Fig. 1). Most samples were recovered from the latter (Punta Sur), where the highest density of individuals is found.
Fig. 1

Location of Guadalupe Island, Baja California, Mexico, and the sites where the sampling was made (Punta Sur, Las casitas, and Corralitos)

Scat analysis

Only fresh scat samples were selected. Three assumptions were made: (1) each sample corresponded to one individual, (2) most samples were from adult females (with or without a pup), as this sex and age class is the second most abundant at the GFS breeding colonies, after pups (Gallo-Reynoso 1994), and (3) based on the long duration of maternal foraging trips (see “Introduction” section), each scat would contain information regarding the last trip of the individual; however, based on the gut passage times (17–44 h) that are known for other otariid species (Dellinger and Trillmich 1988), each scat should represent the most recent 1–2 days of foraging within the last trip.

Scat samples from pups were not collected; these are easily recognizable based on size, consistency, and color. Each scat sample was preserved in a plastic bag labeled with the date and place of collection for posterior processing at the Fish Ecology Laboratory at the Centro Interdisciplinario de Ciencias Marinas of the Instituto Politécnico Nacional (CICIMAR-IPN; Interdisciplinary Center for Marine Sciences of Mexico’s National Polytechnic Institute) in La Paz, Baja California Sur, Mexico. The scat samples were passed through a set of sieves of varying mesh size (2.0, 1.19, and 0.71 µm). The hard structures (beaks and otoliths) were removed and then identified to the lowest possible taxonomic level. The Wolff (1984), and Young et al. (2013) identification guides were consulted to aid in identifying cephalopod beaks; otoliths were identified based on Morrow (1979) and Lowry (2011).

A cumulative diversity curve was used to determine the minimum sample size necessary to represent the GFS diet (Amador-Capitanachi et al. 2017). EstimateS Swin8.2.0 (Colwell 2009) software was used to calculate the mean diversity based on the Shannon–Wiener index and the standard deviation. The coefficient of variation (CV) was calculated to obtain a quantitative estimate of the number of scat samples necessary to adequately represent the population in this analysis. When the CV is less than or equal to 5% (0.05), the number of samples (e.g., scats) analyzed is considered representative of the diet of the population under consideration (Jiménez and Hortal 2003; Amador-Capitanachi et al. 2017).

The importance of each prey species was expressed by the Index of Prey Importance (IIMP), modified by García-Rodríguez and De La Cruz-Agüero (2011), for the trophic analysis of pinnipeds:
$${\text{IIMP}}_{i} = \frac{1}{U}\mathop \sum \limits_{j = 1}^{u} \frac{{x_{ij} }}{{X_{j} }},$$
where x ij is the number of observations of the species i in the scat sample j, Xj is the total identifiable structures in scat sample j, u is the total number of scat samples where taxon i was identified and U is the total number of scat samples. We counted every structure, not accounting for how many individuals of each prey species were in the scat. We acknowledge this could overestimate the importance of certain items; however, this allowed us to compare to other referenced studies that applied the same approach.
The breadth of the GFS trophic spectrum was determined by the Levin´s standardized index (Krebs 1999; Amador-Capitanachi et al. 2017), which is estimated by the following formula:
$$B_{i} = \frac{1}{n - 1}\left( {\frac{1}{{\varSigma_{j} P_{ij} }} - 1} \right),$$
where \(B_{i }\) is the trophic breadth, \(P_{ij}\) is the proportion of prey i in the diet of predator j and \(n\) is the total number of prey species in the diet. Values of B i lower than 0.6 indicate a specialist diet, while values higher than 0.6 indicate a generalist diet (Labropoulou and Eleftheriou 1997).
The GFS diet was determined at both the population and individual levels using Costello’s method (Amundsen et al. 1996). This graphic analysis involves plotting the frequency of occurrence against the specific abundance (number of structures) of each dietary component. The importance of each prey item and the phenotypic contribution to the trophic niche breadth can be interpreted along the diagonals in the plot. Amundsen et al. (1996) distinguished four distinct scenarios depending on the type of consumption (Fig. 2).
Fig. 2

Hypothetical scenarios taken from Amundsen et al. (1996); 1 specialization in different types of prey, 2 a more generalized diet with some individual variation in diet breadth, 3 specialization in one type of prey and the occasional consumption of other species, and 4 a mixed foraging display, where some individuals are more specialist and others employ more generalized foraging habits

To identify possible variations in diet over time, the breeding season was divided into two periods: early (June 15–July 15) and late (July 16–August 15).

The GFS trophic position was calculated by the equation proposed by Christensen and Pauly (1992):
$${\text{TP}} = 1 + \mathop \sum \limits_{j = 1}^{n} {\text{DC}}_{ij} * {\text{TL}}_{j} ,$$
where \(TP\) is the trophic position, \({\text{CD}}_{ij}\) represents the proportion of prey \(j\) in the diet of predator \(i\), \({\text{TL}}_{j}\) is the trophic position of prey species \(j\) and \(n\) is the number of prey in the system.

The trophic position values for species identified in the GFS scats were based on the FishBase database (Froese and Pauly 2015) and additional specialized literature (Mearns et al. 1981; Palomares and Pauly 2015).

Stable isotope analysis

For this analysis, samples were collected from 1- to 2-month-old GFS pups. These individuals were at their initial lactation stage (Gallo-Reynoso 1994) and they had not molted their lanugo; change of pelage starts when they are 4–5-month-old (observation by authors). After physical restraint, an approximately 5 × 5 cm fur sample was taken from the dorsal area of each pup, as close to the base as possible using scissors. The samples were stored in labeled envelopes with all information regarding each collection (e.g., code of sampled individual, date, and site). In the laboratory at CICIMAR-IPN, these were washed using a 1:1 solution of chloroform–methanol to eliminate impurities. Then, each sample was homogenized in an agate mortar. Approximately 1 ± 0.2 mg was taken from each sample and stored in a 5 × 5 mm tin capsule. The samples were analyzed in an isotope ratio mass spectrometer at the Stable Isotopes Laboratory at the University of California in Santa Cruz, USA.

The proportion of stable isotopes of each element is represented using the delta (δ) notation, following the equation proposed by DeNiro and Epstein (1981):
$$\delta^{15} {\text{N}} {\text{or}} \delta^{13} C = 1000\left( {\frac{{R_{\text{sample}} }}{{R_{\text{standard}} }} - 1} \right),$$
where \(R_{\text{sample}}\) is the ratio (15N/14N or 13C/12C) for the sample and \(R_{\text{standard}}\) is the ratio (15N/14N or 13C/12C) for the standard.

The units of measure are expressed as parts per thousand (‰). The internationally recognized standards for these elements are Pee Dee Belemnite (PDB; 0.011‰) for carbon and atmospheric nitrogen (N2; 0.004‰) for nitrogen. Repeated measurements of internal laboratory standards yielded a within-run standard deviation of ≤ 0.2‰ for both δ13C and δ15N.

To identify isotopic subgroups, δ13C and δ15N value distributions were created by multidimensional analysis to construct a Euclidean distance matrix for nonmetric multidimensional scaling (NMDS) ordination. The separation among subgroups was conducted by visual classification. As a next step, a one-way analysis of similarities (ANOSIM) with Euclidean distance in the program PRIMER 6 ® (Clarke and Gorley 2006) was performed to corroborate this differentiation. The SIBER (Stable Isotope Bayesian Ellipses in R) routine in the SIAR (Stable Isotope Analysis for R) package in R was used to determine isotopic niches for each subgroup. This routine consists of using convex polygons to enclose the δ13C and δ15N values for each group. Based on these polygons, the analysis provides Bayesian standard bivariate (δ15N and δ13C) ellipse areas (‰2) corrected (SEAc) for small sample sizes that represent 95% of the variance. These SEAc (subgroups of higher credibility) were generated using Monte Carlo simulations. The area overlap between them was also calculated (R Development Core Team 2008; Jackson et al. 2011). This analysis was carried out for all plotted subgroups, also statistically confirmed via ANOSIM.

The equation of Post (2002) was used to estimate the trophic position based on δ15N:
$${\text{TP}} = \lambda \frac{{\left( {\delta^{15} {\text{N}}_{\text{predator}} - \delta^{15} {\text{N}}_{\text{base}} } \right)}}{{\Delta_{n} }},$$
where \({\text{TP}}\) is the trophic position of predator, \(\lambda\) is the trophic position of the organism used as secondary consumer, and \(\delta^{15} {\text{N}}_{\text{predator}}\) is the value of this stable isotope for the GFS; to have a more accurate result within this equation, we used hypothetical values of adult females based on their sampled pups by subtracting 1‰ from each δ15N value of the latter (Elorriaga-Verplancken et al. 2016b); since these “mothers” values did not originate from direct sampling, we only modified pups δ15N for this particular TP analysis. This correction allowed us to have more accurate values of adult females; however, since females were not actually analyzed, we acknowledge that this modification could be a potential source or error. \(\delta^{15} {\text{N}}_{\text{base}}\) is the δ15N value of the organism used as secondary consumer Sardinops sagax, (12.9‰, Carlisle et al. 2015) and \(\Delta_{n}\) represents the δ15N fractionation value (3.0‰, Hobson et al. 1996).


Scat analysis

During the study period, a total of 107 scat samples were recovered, from which 64 contained hard structures. Cephalopod beaks were the most common hard structure, occurring in 62 scat samples; another common finding was marine grass of the genus Phyllospadix, occurring in 38 scat samples. Only 12 scat samples contained fish otoliths, while two samples contained crustacean remains, possibly from pelagic red crabs Pleuroncodes planipes; however, considering the degree of digestion, the latter were not considered in this analysis.

The CV of the cumulative diversity curve indicated that 47 scat samples was the minimum number required to be representative of the GFS diet.

The trophic spectrum was composed of 12 prey species (four cephalopods and eight fishes), which were identified to the genus level due to the degree of digestion. The most abundant cephalopod group was represented by 398 beaks, while the most common fish was represented by 112 otoliths.

The Index of Importance (IIMP) indicated that the most important prey was the jumbo squid Dosidicus gigas (51%), followed by the hooked squid Onychoteuthis spp. (30%). The enope squid Abraliopsis spp. and the luminous flying squid Eucleoteuthis luminosa together represented 7% of the GFS diet.

In terms of fishes, the lanternfish Symbolophorus spp. was the most important genus at 4%, followed by the Pacific sanddab Citharichthys spp. (2%), the dogtooth fish Ceratoscopelus spp. (1.39%), and the blue lanternfish Tarletonbeania spp. (1.11%). Each one of the remaining genuses represented less than 1% (Table 1).
Table 1

Identified prey species of the Guadalupe fur seal (Arctocephalus philippii townsendi) of the Guadalupe Island (GI); IIMP = Index of importance by prey, P = Pelagic, EP = Epi-pelagic, M = Mesopelagic, and B = Benthic

Common name



Trophic level

# structures


IIMP (100%)


 Jumbo squida

Dosidicus gigas






 Hooked squida

Onychoteuthis spp.






 Enope squidb

Abraliopsis spp.






 Luminous flying squida

Eucleoteuthis luminosa








Symbolophorus spp.






 Pacific sanddabc

Citharichthys spp.






 Dogtooth lampfishc

Ceratoscopelus spp.






 Blue Lanternfishc

Tarletonbeania spp.







Atherinops affinis






 Rock fishc

Sebastes spp.






 California tonguefishc

Symphorus spp.






 California headlight fishc

Diaphus spp.






Otolith NI










References used for the description of trophic position and habitat are included

aPalomares and Pauly (2015)

bMearns et al. (1981)

cFroese and Pauly 2015

*Number of scats with hard structures

Levin’s standardized index indicated a general specialist tendency (B i = 0.19). A lower value was obtained (B i = 0.15) for the first half of the breeding season (June 15–July 15) relative to that for the second half (July 16–August 15) (B i = 0.38).

In addition, the Costello plot with the modification proposed by Amundsen et al. (1996) showed a scenario 4 (a mixed foraging display, where some individuals are more specialist and others employ more generalized foraging habits). The overall most frequent and abundant prey was D. gigas, followed by Onychoteuthis spp., as well as for the first half of the breeding season. In contrast, the abundance of D. gigas was nearly equal to that of Onychoteuthis spp. for the second half of the breeding season; moreover, the presence of the fish Symbolophorus spp. was considerable, although its numbers were lower. The remaining species were rare items in the diet (Fig. 3).
Fig. 3

Costello’s graph. Numerical abundance of prey species by frequency of occurrence within the diet of the Guadalupe fur seal (Arctocephalus philippii townsendi) of the Guadalupe Island. a Overall breeding season; b first half of the breeding season; c second half of the breeding season. Dg = Dosidicus gigas, O = Onychoteuthis spp., S = Symbolophorus spp., all the rest = Abraliopsis spp., Eucleoteuthis luminosa, Ceratoscopelus spp., Atherinops affinis, Citharichthys spp., Diaphus spp., Sebastes spp., Symphorus spp., Tarletonbaeania spp.

The trophic position calculated following the equation published by Christensen and Pauly (1992) was 4.6, making the GFS a tertiary carnivore consumer. This value decreased slightly during the second half of the breeding season (4.5), following the Mearns et al. (1981) criteria.

Stable isotope analysis

During the 2013 breeding season, 98 fur samples were obtained from GFS pups. The mean value (± SD) for δ13C was − 17.6 ± 0.4‰, while that for δ15N was 18.3 ± 0.4‰.

The SIBER analysis indicated a wide dispersion of data points, with an SEAc area of 0.4‰2 and a polygon area of 2‰2 (Fig. 4). A multidimensional analysis revealed three groups; the ANOSIM confirmed significant differences between these groups (R = 0.773, p = 0.001). Group 1 had the lowest mean for both δ13C and δ15N (− 17.8 and 17.8‰, respectively), while Group 2 had a δ13C value equal to that of Group 1, but a distinct δ15N value (− 17.8 and 18.4‰, respectively). Finally, Group 3 presented the highest values for both stable isotopes (δ13C = − 17.1 and δ15N = 18.7‰). The SIBER routine was performed on these groups, indicating no trophic overlap (0) between any of the groups.
Fig. 4

Isotopic groups of Guadalupe fur seals (Arctocephalus philippii townsendi) from Guadalupe Island, based on the analysis of pups’ fur, as proxies for maternal foraging. Arrows indicate probable trends in terms of trophic position and habitat use of the different groups. Dotted lines represent the Convex Hull areas (polygons), while the subgroups within are formed by the standard ellipse areas corrected for small sample sizes (SEAc), provided by SIBER analysis

Based on Post’s (2002) algorithm, the overall GFS trophic position was 4.5, making this species a tertiary carnivore consumer. The trophic positions among groups were slightly different (Group 1 = 4.3, Group 2 = 4.5, and Group 3 = 4.6).


The GFS was identified as a primarily teutophagous consumer, as reported previously (Gallo-Reynoso and Esperón-Rodríguez 2013). However, our study is the first to simultaneously employ complementary techniques to reveal the presence of different diets in their primary colony during early and late breeding season using scat analysis (information of the last foraging trip by individuals); we also identified different foraging habits during 3–4 months prior to sample collection via isotopic analysis in fur, distinguishing three groups with distinct trends. The GFS is a species that can travel large distances (up to 600 km) during its foraging trips (Gallo-Reynoso et al. 2008), facilitating this apparent inter-individual foraging diversification.

Scat analysis

The size of the sample assessed here was sufficient to adequately represent the diet of the colony’s most abundant independent consumer class (adult females) during the last foraging trips made by the individuals sampled during the breeding season. Our findings are an important contribution regarding this technique, as previous studies on the diet of GFSs from Guadalupe Island were mostly based on small sample sizes (Gallo-Reynoso and Esperón-Rodríguez 2013).

The GFS diet was composed of a small number of species (N = 12) and included a higher richness of fish species than cephalopod species. However, cephalopods were most important to the diet (89%). This teutophagous tendency has been reported previously for GFSs (Gallo-Reynoso and Esperón-Rodríguez 2013) as well as for species of the genus Arctocephalus and other species with oceanic habits (Fiscus 1982). In our study, the main prey reported for GFSs was the jumbo squid D. gigas, as also evidenced by Amador-Capitanachi et al. (2017) for this colony. This prey species has also been reported previously in other studies (Gallo-Reynoso 1994; Hanni et al. 1997; Gallo-Reynoso et al. 2005; Aurioles-Gamboa and Camacho-Ríos 2007; Hernández 2009; Esperón Rodriguez and Gallo-Reynoso 2012); however, its importance was lower and varied. Onychoteuthis spp. was the second most important prey identified by our study; while other studies have identified this species as the main prey of this fur seal (Gallo-Reynoso 1994; Gallo-Reynoso et al. 2005).

Cephalopod beaks were the most frequent hard structure recovered from the scat samples examined in this study; however, in this and previous studies, the quantity of beaks may be biased by the size of these structures as well as by their chitin composition, which resists digestion leading to the accumulation of these structures in the stomachs of predators (Tollit et al. 1997; Bowen 2000; Arim and Naya 2003), and possibly provoking regurgitation (Sinclair et al. 1994; Casper et al. 2006; Gallo-Reynoso and Esperón-Rodríguez 2013). Regurgitation has been observed in some terrestrial mammals and in GFSs (Aurioles-Gamboa and Camacho-Ríos 2007; Hernández 2009); a facilitation for this purging process may explain the large quantities of marine grasses of the genus Phyllospadix identified in the scat samples, together with the cephalopod beaks or remains, as well as the regurgitated matter observed in the field during sample collection.

The importance of fish species to the GFS diet was low for the season and class that were sampled; most were from the Myctophidae family, which has been identified elsewhere as important prey for pelagic predators with nocturnal habits that may take advantage of vertical migrations (Choy et al. 2012; Stewart et al. 2014). Other groups of fish were rare in the diet, including tonguefish (Symphorus spp.) and rockfish (Sebastes spp.), which have a primarily coastal distribution (Nelson et al. 2004). This study involved scats from breeding sites and the majority of our samples were presumed to come from adult females. However, we do not discard the presence of juveniles’ scats. GFSs of this age class have been sighted near the continental shelf (Weber and Roletto 1987, Lander 2000), which would explain the presence of coastal items in a few scats. Additional telemetry research is necessary to identify location differences between adults and juveniles.

Prior to the present study, the GFS foraging strategy had been classified as specialist (Gallo-Reynoso and Esperón-Rodríguez 2013), which is consistent with our results. However, by reexamining the GFS foraging trends (Amundsen et al. 1996), our study is the first to confirm a diversity of diets consumed by distinct individuals within the same colony. The primary prey was clearly cephalopods; however, not all individuals consumed the same species. Moreover, the comparison between the two periods of the breeding season (June through mid-July and mid-July through August) revealed temporal variation in diet, with a slight increase in main prey diversity during the late breeding season. We do not discard this change could be due to age or size of females. Older and more experienced female fur seals of other species (northern fur seal, Callorhinus ursinus and Antarctic fur seal, Arctocephalus gazella) usually get to the colonies and give birth earlier in the breeding season, relative to younger ones (Lunn and Boyd 1993; Boltnev and York 2001). Foraging differences in relation to age or experience of individuals have been suggested before, for the northern fur seal (Kurle and Worthy 2001) and the Australian sea lion (Neophoca cinerea) (Hoskins et al. 2015). Since additional evidence is required in regard to the effect of experience on GFSs, this hypothesis should be taken with high caution and other explanations such as changes in the abundance of prey species across the breeding season or changes in energetic requirements of adult females cannot be discarded.

Another relevant aspect is the change in the main prey between another recent study on GFSs (Hernández 2009) and the present one (as well as Amador-Capitanachi et al. 2017); Hernández (2009) identified the opalescent squid Doryteuthis opalescens as the primary prey, whereas in the present study, D. gigas was the main prey. This change may be attributed to two possibly complementary factors: (1) a decrease in D. opalescens biomass as a result of commercial fishing (Denis et al. 2002), and (2) an increase in D. gigas biomass during the last decade (Wing 2005; Field et al. 2007). Data from Mexico’s Comisión Nacional de Acuacultura y Pesca (CONAPESCA; National Commission of Aquaculture and Fisheries) show a marked increase in the capture of this squid for the study area, from 500 kg in July 2006 (Hernández 2009) to 93,599 kg in 2013. The shift in the most important prey to focus on a more abundant resource suggests an opportunistic foraging strategy (Gerking 1994) for the GFS once a broad time scale (i.e., years) is assessed.

The trophic position identified in this study (4.5–4.6) was higher than previously reported (e.g., 3.9–4.3) (Pauly et al. 1998; Aurioles-Gamboa and Camacho-Ríos 2007; Hernández 2009; Pablo 2009). This is due to the higher percentage of D. gigas in the diet in the present study. This large squid has a high trophic position (~ 3.9) as it is a voracious predator that primarily consumes fish (Myctophidae), and in smaller proportions mollusks (cephalopods, including other squids) and crustaceans (decapods) (Markaida and Sosa-Nishizaki 2003; Field et al. 2007; Stewart et al. 2014).

Stable isotope analysis

The distinct isotopic groups displayed (via SIBER and ANOSIM) notable intra-species variability that apparently reflects unique foraging habits. This finding has been reported previously as an intra-population strategy that reduces competition between conspecifics in the presence of low inter-specific pressure (Van Valen 1965; Bolnick et al. 2003). These GFS isotopic variations during the 3–4 months prior to fur sample collection could be characterized as follows: Group 1 had a lower trophic position (δ15N) than either Groups 2 or 3; however, baseline differences (instead of dietary) related specific foraging locations cannot be discarded. Additionally, Group 3 displayed more probable nearshore habits (δ13C) than either Groups 1 or 2. In this regard, at least one portion of the GFS population has been suggested to feed near the coast (Amador-Capitanachi et al. 2017), while a vast majority accomplishes offshore foraging trips (Gallo-Reynoso et al. 2008). This isotopic timeframe is mostly reflected by a period before the breeding season in summer, when females are mostly absent from their breeding site (Gallo-Reynoso 1994), because they are performing intense foraging trips (Amador-Capitanachi 2018).

Our results only assessed one age and sex class (adult females via the sampled pups), but this is the most abundant age and sex class (independent consumer) at the colony. However, future studies should include other classes of this population. A small preliminary fur sampling, in this Guadalupe colony, during the 2014 breeding season that included ten adult female and five adult male GFSs, evidenced higher isotope values (δ15N = 17.5 ± 0.7‰ vs. 17 ± 0.1‰, δ13C = − 16.8 ± 0.5‰ vs. − 17.6 ± 0.4‰) in the latter, suggesting a possible trophic variation between sexes in terms of trophic position and habitat use (Elorriaga-Verplancken and Juárez-Ruiz unpublished data). These interpretations of inter-sex variation should be considered with caution due to the small sample size and probable differences regarding molt strategies between males and females; thus, we only focus on our results pertaining to adult females as examined through their pups.

There is abundant evidence regarding foraging variation between conspecific marine mammals of the same sex, as is the case with sea otters Enhydra lutris (Estes et al. 2003), Southern elephant seals Mirounga leonina (Lewis et al. 2006), Northern elephant seals Mirounga angustirostris (Simmons et al. 2007; Velázquez and Elorriaga-Verplancken 2017), Galapagos sea lions Zalophus wollebaeki (Páez-Rosas and Aurioles-Gamboa 2010), California sea lions Zalophus californianus (Elorriaga-Verplancken et al. 2013), and particularly fur seals, such as the Antarctic fur seal Arctocephalus gazella (Staniland and Boyd 2003; Kernaléguen et al. 2015), the Northern fur seal Callorhinus ursinus (Robson et al. 2004), and the subantarctic fur seal Arctocephalus tropicalis (Kernaléguen et al. 2015). Our study is the first to report this strategy for GFSs.

The results of both techniques were complementary, particularly considering the parity of values for the trophic positions (4.6 and 4.5, tertiary carnivore consumer). Despite the fact that both approaches assess different time frames (3–4 months for stable isotopes vs. days for scat samples), both identified distinct foraging groups and predominantly low δ13C values, reflecting oceanic habits typical of teutophagous predators (Burton and Koch 1999; Elorriaga-Verplancken et al. 2016a) within a species-prey (squid) foraging tendency that was corroborated by the scat analysis. Some higher δ13C values were also detected, likely due to the presence of occasional coastal prey in scat samples.

This species should continue to be monitored, as our sample collection occurred before the period of anomalous warming in the northeast Pacific (Kintisch 2015), which had a considerable impact on GFSs from the San Benito Archipelago, Mexico (Elorriaga-Verplancken et al. 2016a). We also recommend the use of mixing models to determine the relative abundance of prey species contributing to this predator’s isotopic signal. It is also important to monitor the diet and isotopic baseline values corresponding to specific areas during different seasons, as our study focused solely on the breeding season and the 3–4 months that preceded it. To isotopically assess a longer period (at least 2 years), including seasonal variability (Lowther et al. 2013), we suggest analyzing stable isotopes in GFS whiskers in future studies.

Our study contributes important and relevant information not previously reported regarding the foraging diversity exhibited by this species, which originates entirely from our study area (the number of births at San Benito Archipelago is insignificant; Elorriaga-Verplancken et al. 2016a). It is particularly important to understand the foraging habits of the GFS as it exemplifies the adaptive strategies utilized by a species in recovery, considered extinct 70–80 years ago (Hubbs 1956), including the conformation of specialist groups that are able to co-exist (Estes et al. 2003), within a scenario proposed by Weber et al. (2004), in which extrinsic factors such as resource availability will be transcendental for this species’ long-term success.



We thank the Secretaría de Medio Ambiente y Recursos Naturales through the Dirección General de Vida Silvestre en México for granting us research permit SGPA/DGVS/11744/13, as well as Comisión Nacional de Áreas Naturales Protegidas (CONANP)– Reserva de la Biósfera Isla Guadalupe. We also thank Secretaría de Marina (SEMAR; Mexican Navy) and the Cooperativa pesquera “Abuloneros y Langosteros de Isla Guadalupe” (fishermen society in Guadalupe Island), for their support in the field. FREV and XGMS thank IPN for the received support through the Contracting Excellence Program and fellowship EDI. We also thank Kristin Sullivan for editing the English version of the manuscript.

Compliance with ethical standards


Financial support was provided by CONACYT Cencia Básica- Project 181876 and SIP-20130944 from Instituto Politécnico Nacional (IPN).

Conflict of interest

The authors declare that they have no conflict of interest, of any kind.

Human and animal rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.


  1. Amador-Capitanachi MJ, Moreno-Sánchez XG, Juárez-Ruiz A, Ferretto G, Elorriaga-Verplancken FR (2017) Trophic variation between the two existing Guadalupe fur seal colonies on Guadalupe Island and the San Benito Archipelago, Mexico. Aquat Mammal 43:14–25. CrossRefGoogle Scholar
  2. Amador-Capitanachi MJ (2018) Nicho isotópico interanual (2013-2016) y análisis del desplazamiento mediante telemetría en el lobo fino de Guadalupe (Arctocephalus philippii townsendi). MSc dissertation. CICIMAR-IPN, La Paz, BCS, MexicoGoogle Scholar
  3. Amundsen PA, Gabler HM, Staldvik FJ (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. CrossRefGoogle Scholar
  4. Arim M, Naya DE (2003) Pinniped diets inferred from scats: analysis of biases in prey occurrence. Can J Zool 81:67–73. CrossRefGoogle Scholar
  5. Aurioles-Gamboa D, Camacho-Ríos FJ (2007) Diet and feeding overlap of two Otariids, Zalophus californianus and Arctocephalus townsendi: implications to survive environmental uncertainty. Aquat Mammal 33:315–326. CrossRefGoogle Scholar
  6. Aurioles-Gamboa D, Elorriaga-Verplancken FR, Hernández CJ (2010) The current population status of Guadalupe fur seal (Arctocephalus townsendi) on the San Benito Islands, Mexico. Mar Mammal Sci 26:402–408. CrossRefGoogle Scholar
  7. Bolnick DI, Svanbäck R, Fordyce JA, Yang LH, Davis JM, Hulsey C, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. CrossRefPubMedGoogle Scholar
  8. Boltnev AL, York AE (2001) Maternal investment in northern fur seals (Callorhinus ursinus): interrelationships among mothers’ age, size, parturition date, offspring size and sex ratios. J Zool (London) 254:219–228. CrossRefGoogle Scholar
  9. Bowen WD (2000) Reconstruction of pinniped diets: accounting for complete digestion of otoliths and cephalopod beaks. Can J Fish Aquat Sci 57:898–905. CrossRefGoogle Scholar
  10. Burton RK, Koch PL (1999) Isotopic tracking of foraging and longdistance migration in northeastern Pacific pinnipeds. Oecologia 119:578–585. CrossRefPubMedGoogle Scholar
  11. Carlisle AB, Goldman KJ, Litvi SY, Madigan DJ, Bigman JS, Swithenbank AM, Kline TC, Block BA (2015) Stable isotope analysis of vertebrae reveals ontogenetic changes in habitat in an endothermic pelagic shark. Proc R Soc B 282:20141446. CrossRefPubMedPubMedCentralGoogle Scholar
  12. Casper RM, Gales NJ, Hindell MA, Robinson SM (2006) Diet estimation based on an integrated mixed prey feeding experiment using Arctocephalus seals. J Exp Mar Bio Ecol 328:228–239. CrossRefGoogle Scholar
  13. Choy CA, Davison PC, Drazen JC, Flynn A, Gier EJ, Hoffman JC, McClain-Counts JP, Miller TW, Popp BN, Ross SW, Sutton TT (2012) Global trophic position comparison of two dominant mesopelagic fish families (Myctophidae, Stomiidae) using amino acid nitrogen isotopic analyses. PLoS One 7:e50133. CrossRefPubMedPubMedCentralGoogle Scholar
  14. Christensen V, Pauly D (1992) ECOPATH II—a software for balancing steady-state ecosystem models and calculating network characteristics. Ecol Modell 61:169–185. CrossRefGoogle Scholar
  15. Clarke KR, Gorley RN (2006) PRIMER v6 User Manual/Tutorial. Primer-E, Plymouth, UKGoogle Scholar
  16. Colwell RK (2009) EstimateS: statistical estimation of species richness and shared species from samples: user’s guide and application. Accessed 13 Jan 2015
  17. da Silva J, Neilson DL (1985) Limitations of using otoliths recovered in scats to estimate prey consumption in seals. J Fish Aquat Sci 42:1439–1442. CrossRefGoogle Scholar
  18. Dellinger T, Trillmich F (1988) Estimating diet composition from scat analysis in otariid seals (Otariidae): is it reliable? Can J Zool 66:1865–1870. CrossRefGoogle Scholar
  19. DeNiro MJ, Epstein S (1981) Influence of the diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–353. CrossRefGoogle Scholar
  20. Denis V, Lejeune L, Robin JP (2002) Spatio-temporal analysis of commercial trawler data using General Additive models: patterns of Loliginid abundance in the north-east Atlantic. ICES J Mar Sci 59:633–648. CrossRefGoogle Scholar
  21. Elorriaga-Verplancken F, Aurioles-Gamboa D, Newsome SD, Martínez-Díaz SF (2013) δ15N and δ13C values in dental collagen as a proxy for age- and sex-related variation in foraging strategies of California sea lions. Mar Biol 160:641–652. CrossRefGoogle Scholar
  22. Elorriaga-Verplancken FR, Sierra-Rodríguez G, Rosales-Nanduca H, Acevedo-Whitehouse K, Sandoval-Sierra J (2016a) Impact of the 2015 El Niño-Southern Oscillation on the abundance and foraging habits of Guadalupe fur seals and California sea lions from the San Benito Archipelago, Mexico. PLoS One 11:e0155034. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Elorriaga-Verplancken FR, Juárez-Ruiz A, Baleytó MA, Galván-Magaña F, Aguíñiga-Farcía S (2016b) Isotopic variation between adult female Guadalupe fur seals and their offspring: implications for the use of neonates as proxies for maternal foraging. Aquat Mammal 42:268–276. CrossRefGoogle Scholar
  24. Esperón Rodriguez M, Gallo-Reynoso JP (2012) Analysis of the recolonization of San Benito Archipelago by Guadalupe fur seals (Arctocephalus townsendi). Lat Am J Aquat Res 40:213–223. CrossRefGoogle Scholar
  25. Estes JA, Riedman ML, Staedler MM, Tinker MT (2003) Individual variation in prey selection by sea otters: Patterns, causes and implications. J Anim Ecol 72:144–155. CrossRefGoogle Scholar
  26. Field JC, Baltz KEN, Walker W (2007) Range expansion and trophic interactions of the Jumbo Squid, Dosidicus Gigas, in the California current. Calif Coop Ocean Fish Investig Rep 48:131–146Google Scholar
  27. Fiscus CH (1982) Predation by marine mammals on squids of the eastern North Pacific Ocean and the Bering Sea. Mar Fish Rev 44:1–10Google Scholar
  28. Froese F, Pauly D (2015) Accessed 12 Apr 2015
  29. Gallo-Reynoso JP (1994) Factors affecting the population status of Guadalupe Fur Seal, Arctocephalus Townsendi (Merriam 1897) at Isla De Guadalupe, Baja California, Mexico. PhD Dissertation, University of California, Santa Cruz, CaliforniaGoogle Scholar
  30. Gallo-Reynoso JP, Esperón-Rodríguez M (2013) Diet composition of the Guadalupe fur seal (Arctocephalus townsendi). Where and what do they eat? Mar Freshw Behav Physiol 46:455–467. CrossRefGoogle Scholar
  31. Gallo-Reynoso JP, Le Boeuf BJ, Figueroa-Carranza AL, Maravilla-Chávez O (2005) Los pinnípedos de Isla Guadalupe. In: Peters E (ed) Santos del Prado K. Instituto Nacional de ecología, SEMARNAT, Mexico City, pp 171–201Google Scholar
  32. Gallo-Reynoso JP, Figueroa-Carranza AL, Le Boeuf BJ (2008) Foraging behavior of lactating Guadalupe fur seal females. In: Espinoza E, Ortega J (eds) Lorenzo C. Advances in the study of mammals in Mexico, Mexico City, pp 595–614Google Scholar
  33. García-Capitanachi B, Schramm Y, Heckel G (2017) Population Fluctuations of Guadalupe Fur Seals (Arctocephalus philippii townsendi) Between the San Benito Islands and Guadalupe Island, Mexico, During 2009 and 2010. Aquat Mammals 43(5):492–500CrossRefGoogle Scholar
  34. García-Rodríguez F, De La Cruz-Agüero J (2011) A comparison of indexes for prey importance inferred from otoliths and cephalopod beaks recovered from pinniped scats. J Fish Aquat Sci 6:186–193.
  35. Gerking SD (1994) Feeding ecology of fish. Academic, San DiegoGoogle Scholar
  36. Habran S, Debier C, Crocker DE, Houser DS, Lepoint G, Bouquegneau JM, Das K (2010) Assessment of gestation, lactation and fasting on stable isotope ratios in northern elephant seals (Mirounga angustirostris). Mar Mammal Sci 26:880–895. CrossRefGoogle Scholar
  37. Hanni KD, Long DJ, Jones RE, Pyle P, Morgan LE (1997) Sightings and strandings of Guadalupe Fur seals in Central and Northern California, 1988–1995. J Mammal 78:684–690. CrossRefGoogle Scholar
  38. Hernández J (2009) Distribución, abundancia y estructura alimentaria del lobo fino de Guadalupe (Arctocephalus townsendi) en Isla Guadalupe, México. MSc dissertation, Centro de Investigación Científica y Educación Superior de Ensenada, Ensenada Baja California, MexicoGoogle Scholar
  39. Hobson KA, Welch HE (1992) Determination of trophic relationships within a high arctic marine food web using δ13C and δ15N analysis. Mar Ecol Prog Ser 84:9–18CrossRefGoogle Scholar
  40. Hobson KA, Schell DM, Renouf D, Noseworthy E (1996) Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals. Can J Fish Aquat Sci 53:528–533. CrossRefGoogle Scholar
  41. Hoskins AJ, Costa DP, Wheatley KE, Gibbens JR, Arnould JPY (2015) Influence of intrinsic variation on foraging behaviour of adult female Australian fur seals. Mar Ecol Prog Ser 526:227–238. CrossRefGoogle Scholar
  42. Hubbs CL (1956) The Guadalupe fur seal still lives! Zoonooz 29:6–9Google Scholar
  43. Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—stable isotope Bayesian ellipses in R. Anim Ecol 80:595–602. CrossRefGoogle Scholar
  44. Jiménez VA, Hortal J (2003) Las curvas de acumulación de especies y la necesidad de evaluar la calidad de los inventarios biológicos. Rev Ibérica Arac 8:151–161Google Scholar
  45. Kernaléguen L, Arnould JPY, Guinet C, Cherel Y (2015) Determinants of individual foraging specialization in large marine vertebrates, the Antarctic and subantarctic fur seals. J Anim Ecol 84:1081–1091. CrossRefPubMedGoogle Scholar
  46. Kintisch E (2015) “The Blob” invades Pacific, flummoxing climate experts. Science. CrossRefPubMedGoogle Scholar
  47. Krebs C (1999) Ecological methodology, 2nd edn. Addison-Wesley Educational Publishers Inc, Menlo ParkGoogle Scholar
  48. Kurle CM, Worthy GAJ (2001) Stable isotope assessment of temporal and geographic differences in feeding ecology of northern fur seals (Callorhinus ursinus) and their prey. Oecologia 126:254–265. CrossRefPubMedGoogle Scholar
  49. Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. J Fish Biol 50:324–340. CrossRefGoogle Scholar
  50. Lander M (2000) Satellite tracking a rehabilitated Guadalupe fur seal (Arctocephalus townsendi). Aquat Mammal 26:137–142Google Scholar
  51. Lewis R, O’Connell TC, Lewis M, Campagna C, Hoelzel AR (2006) Sex-specific foraging strategies and resource partitioning in the Southern elephant seals (Mirounga leonina). Proc R Soc B 273:2901–2907. CrossRefPubMedPubMedCentralGoogle Scholar
  52. Lowry MS (2011) Photographic catalog of California marine fish otoliths: prey of California sea lions (Zalophus californianus) (NMFSTechnical Memorandum) NOAA, pp 256Google Scholar
  53. Lowther AD, Harcourt RG, Page B, Goldsworthy SD (2013) Steady as he goes: at-sea movement of adult male Australian sea lions in a dynamic marine environment. PLoS One 8:e74348. CrossRefPubMedPubMedCentralGoogle Scholar
  54. Lunn NJ, Boyd IL (1993) Effects of maternal age and condition on parturition and the perinatal period of Antarctic fur seals. J Zool 229:55–67. CrossRefGoogle Scholar
  55. Markaida U, Sosa-Nishizaki O (2003) Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. J Mar Biol Assoc UK 83:507–522. CrossRefGoogle Scholar
  56. McClatchie S, Field J, Thompson AR, Gerrodette T, Lowry M, Fiedler PC, Nieto KM, Vetter RD (2016) Food limitation of sea lion pups and the decline of forage off central and southern California. R Soc Open Sci 3:150628. CrossRefPubMedPubMedCentralGoogle Scholar
  57. Mearns A, Olson R, Young D, Schafer H (1981) Trophic structure and the cesium-potassium ratio in pelagic ecosystems. CalCOFI Rep 22:99–110Google Scholar
  58. Minagawa M, Wada E (1984) Stepwise enrichment of N along food chains: further evidence and the relation between δ15N and animal age. Geachimica Cosmochim Acta 48:1135–1140. CrossRefGoogle Scholar
  59. Morrow JE (1979) Preliminary keys to otoliths of some adult fishes of the Gulf of Alaska, Bering Sea, and Beaufort Sea (NMFS Technical Report 420) U.S. Department of Commerce, NOAA, pp 32Google Scholar
  60. Nelson JS, Espinosa-Pérez H, Findley LT, Gilbert CR, Lea RN, Mandrak NE, Williams JD (2004) Common and scientific names of fishes from the United States, Canada, and Mexico. Am Fish Soc, special publication 29Google Scholar
  61. Newsome SD, Del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436. CrossRefGoogle Scholar
  62. Orr AJ, VanBlaricom GR, DeLong RL, Cruz-Escalona VH, Newsome SD (2011) Intraspecific comparison of diet of California sea lions (Zalophus californianus) assessed using fecal and stable isotope analyses. Can J Zool 89:109–122. CrossRefGoogle Scholar
  63. Pablo N (2009) Amplitud, nivel y superposición trófica de los pinnípedos de Islas San Benito, BC, México. MSc dissertation. CICIMAR IPN, La Paz, BCS, MexicoGoogle Scholar
  64. Páez-Rosas D, Aurioles-Gamboa D (2010) Alimentary niche partitioning in the Galapagos sea lion, Zalophus wollebaeki. Mar Biol 157:2769–2781. CrossRefGoogle Scholar
  65. Palomares MLD, Pauly D (2015) World Wide Web electronic publication. Accessed 14 Feb 2015
  66. Pauly D, Trites AW, Capuli E, Christensen V (1998) Diet composition and trophic levels of marine mammals. ICES J Mar Sci 55:467–481. CrossRefGoogle Scholar
  67. Pierce GJ, Boyle PR (1991) A review of methods for diet analysis in piscivorous marine mammals. Oceanogr Mar Biol 29:409–486Google Scholar
  68. Porras-Peters H, Aurioles-Gamboa D, Cruz-Escalona VH, Koch PL (2008) Trophic level and overlap of sea lions (Zalophus californianus) in the Gulf of California, Mexico. Mar Mammal Sci 24:554–576. CrossRefGoogle Scholar
  69. Post DM (2002) Using stable isotopes to estimate trophic position models methods, and assumptions. Ecology 83:703–718. CrossRefGoogle Scholar
  70. R Development Core Team (2008) R: a language and environment for statistical computing. R foundation for statistical computing. Accessed 12 Apr 2015
  71. Robson BW, Michael E, Goebel J, Ream RR, Loughlin TR, Francis RC, Costa DP et al (2004) Separation of foraging habitat among breeding sites of a colonial marine predator, the northern fur seal (Callorhinus ursinus). Can J Zool 82:20–29. CrossRefGoogle Scholar
  72. SEMARNAT, Secretaría de Medio Ambiente y Recursos Naturales (2010) Norma Oficial Mexicana NOM-059 SEMARNAT-2010. Diario Oficial de la Federación (DOF). Accessed 1 Oct 2016Google Scholar
  73. Simmons SE, Crocker DE, Kudela RM, Costa DP (2007) Linking foraging behaviour of the northern elephant seal with oceanography and bathymetry at mesoscales. Mar Ecol Prog Ser 346:265–275. CrossRefGoogle Scholar
  74. Sinclair EH, Loughlin T, Pearcy W (1994) Prey selection by northern fur seals (Callorhinus ursinus) in the eastern Bering Sea. Fish Bull 92:144–156Google Scholar
  75. Staniland IJ, Boyd IL (2003) Variation in the for-aging location of Antarctic fur seals (Arctocephalus gazella) and the effects on diving behavior. Mar Mammal Sci 19:331–343. CrossRefGoogle Scholar
  76. Stewart JS, Hazen EL, Bograd SJ, Byrnes JEK, Foley DG, Gilly WF, Robison BH, Field JC (2014) Combined climate- and prey-mediated range expansion of Humboldt squid (Dosidicus gigas), a large marine predator in the California Current System. Glob Chang Biol 20:1832–1843. CrossRefPubMedGoogle Scholar
  77. Tollit DJ, Steward MJ, Thompson PM, Pierce GJ, Santos MB, Hughes S (1997) Species and size differences in the digestion of otoliths and beaks: implications for estimates of pinniped diet composition. Can J Fish Aquat Sci 54:105–111CrossRefGoogle Scholar
  78. Van Valen L (1965) Morphological variation and width of ecological niche. Am Nat 99:377–389. CrossRefGoogle Scholar
  79. Vander Zanden HB, Bjorndal KA, Reich KJ, Bolten AB (2010) Individual specialists in a generalist population: results from a long-term stable isotope series. Biol Lett 6:711–714. CrossRefPubMedPubMedCentralGoogle Scholar
  80. Velázquez CM, Elorriaga-Verplancken FR (2017) Isotopic evidence for intersexual foraging variation in northern elephant seals from Baja California. Mexico. Mar Biol 164:168. CrossRefGoogle Scholar
  81. Weber MA, Roletto J (1987) Two Recent Occurrences of the Guadalupe fur seal Arctocephalus townsendi in Central California. Bull South Calif Acad Sci 86:159–163Google Scholar
  82. Weber DS, Stewart BS, Lehman N (2004) Genetic consequences of a severe population bottleneck in the Guadalupe fur Seal (Arctocephalus townsendi). J Hered 95:144–153. CrossRefPubMedGoogle Scholar
  83. Wing BL (2005) Unusual invertebrates and fish observed in the Gulf of Alaska, 2004–2005. PICES Press 142:26–28Google Scholar
  84. Wolff G (1984). Identification and estimation of size from the beaks of 18 species of cephalopods from the Pacific Ocean (NMFS Technical Report 17). U.S. Department of Commerce, NOAA, Washington, DC, pp 50Google Scholar
  85. Young RE, Vecchione M, Mangold KM (2013) The tree of life web project. Accessed 28 Feb 2017

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ariadna Juárez-Ruiz
    • 1
  • Fernando R. Elorriaga-Verplancken
    • 1
  • Xchel G. Moreno-Sánchez
    • 1
  • Sergio Aguíniga-García
    • 2
  • María José Amador-Capitanachi
    • 1
  • Casandra Gálvez
    • 1
  1. 1.Instituto Politécnico Nacional-Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN)Departamento de Pesquerías y Biología MarinaLa PazMéxico
  2. 2.Instituto Politécnico Nacional-Centro Interdisciplinario de Ciencias Marinas (CICIMAR-IPN), Departamento de OceanologíaLa PazMéxico

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