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Trophic Level and Overlap of Sea Lions (Zalophus Californianus) in the Gulf of California, Mexico

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Trophic Level and Overlap of Sea Lions (Zalophus Californianus) in the Gulf of California, Mexico MARINE MAMMAL SCIENCE, 24(3): 554–576 (July 2008) C 2008 by the Society for Marine Mammalogy DOI: 10.1111/j.1748-7692.2008.00197.x Trophic level and overlap of sea lions (Zalophus californianus) in the Gulf of California, Mexico HEIDI PORRAS-PETERS DAVID AURIOLES-GAMBOA Laboratorio de Ecologıa´ de Pinnıpedos´ “Burney J. Le Boeuf,” Centro Interdisciplinario de Ciencias Marinas, Instituto Politecnico´ Nacional, Ave. IPN s/n Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur, Mexico´ 23096 E-mail: [email protected] VICTOR HUGO CRUZ-ESCALONA Laboratorio de Dinamica´ y Manejo de Ecosistemas Acuaticos,´ Centro Interdisciplinario de Ciencias Marinas, Instituto Politecnico´ Nacional, Ave. IPN s/n Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur, Mexico´ 23096 PAUL L. KOCH Department of Earth & Planetary Sciences, University of California, Santa Cruz, California 95064, U.S.A. ABSTRACT Stable isotope and scat analyses were used in concert to determine trophic level and dietary overlap among California sea lions from different rookeries in the Gulf of California. Isotopic analysis of the fur of sea lion pups revealed differences in ␦15N and ␦13C values among rookeries during the breeding season. Mean ␦15N and ␦13C values varied from 20.2‰ to 22.4‰ and from −15.4‰ to −14.0‰, respectively. The pattern of differences among rookeries was similar between years in most cases. Isotopic variations among rookeries were associated with differences in prey consumption. There was a significant correlation between ␦15N value and trophic level, as determined by scat analysis. Joint application of isotopic and scat analyses allowed us to identify how the feeding habits of sea lions vary with location. Our results suggest the presence of spatial structure in available prey as well as the localized use of prey by sea lions across the Gulf of California. Key words: California sea lion, Zalophus californianus, Gulf of California, stable isotopes, trophic level, diet. 554 PORRAS-PETERS ET AL.: CALIFORNIA SEA LIONS 555 Thirteen California sea lion (Zalophus californianus) rookeries occur in the Gulf of California, with 10 located north of 28◦N where sardine and anchovy are most abun- dant (Aurioles-Gamboa and Zavala-Gonzalez´ 1994). Adult females exhibit strong philopatry (Hernandez-Camacho´ 2001), and feeding habits seem to show a regional structure (Garcı´a Rodrı´guez and Aurioles-Gamboa 2004). This is particularly true for animals from rookeries that are in close proximity and that overlap in their potential foraging space (Kuhn 2006). Several studies conducted in the Gulf of California have shown that sea lions consume a broad variety of prey and that dietary differences exist among rookeries (Aurioles-Gamboa et al. 1984, Orta-Davila´ 1988, Sanchez-´ Arias 1992, Gutierrez´ 2003). These studies have not been conducted at all major rookeries, however, and they were done at different time periods, so differences ob- served among rookeries might be due to temporal shifts affecting all rookeries. These studies used scat analyses, which offer invaluable, detailed information on prey con- sumption. Yet quantitative assessment of diet using scat analysis is subject to various well-known biases (da Silva and Neilson 1985, Dellinger and Trillmich 1988, Pierce and Boyle 1991, Cotrell et al. 1996, Tollit et al. 1997, Bowen 2000, Orr and Harvey 2001). Stable isotope analysis offers less detailed information on dietary composition than scat analysis, but because it provides information on assimilated food, it avoids some of the biases in scat analysis (Tieszen et al. 1983, Hobson et al. 1994, Holst et al. 2001). Moreover, because the turnover rates of elements in consumer tissues vary according to the metabolic rate of those tissues, stable isotope analysis can integrate dietary information over different time periods (Dalerum and Angerbjorn¨ 2005). Stable isotopes of elements in metabolically inactive tissues (e.g., fur, feathers, skin, and nails) do not turn over, and therefore reflect the diet or body chemistry of an individual during a limited period of tissue formation (Tieszen et al. 1983). Tissues of consumers tend to become enriched in 13C and 15N relative to those of their prey, a process referred to as fractionation or trophic enrichment. The 13C- enrichment per trophic step is roughly + 0.5‰ to + 2‰, based on studies of different tissues of seals and other marine mammals (Kelly 2000, Lesage et al. 2002). The 15N- enrichment ranges from + 2‰ to + 5‰ per trophic step (Schoeninger and DeNiro 1984, Hobson et al. 1996, Kelly 2000). Both carbon and nitrogen isotope values may vary spatially in primary producers because of regional differences in factors such as nutrient or light levels, types of pri- mary producer, or the isotopic composition of carbon and nitrogen substrates (which might vary with the intensity of upwelling or the magnitude of fluvial or atmo- spheric inputs). Because of these effects, carbon isotope values differ between inshore vs. offshore and between benthic vs. pelagic food webs, with lower values in off- shore/pelagic systems, and higher values in inshore/benthic systems (McConnaughey and McRoy 1979, Rau et al. 1983, Hobson et al. 1994, France 1995). There are latitudinal differences in the nitrogen isotope composition of primary producers at the base of food webs in the Gulf of California, with higher values north and lower values south of the Midriff Region (Fig. 1) (Altabet et al. 1999). In addition, because of strong trophic 15N-enrichement, nitrogen isotope values are a reliable indicator of the relative trophic level of organisms within a food chain (Owens 1987, Kelly 2000). Stable isotope analysis of sea lion fur may allow us to examine the spatial structure of foraging by animals from different rookeries. If sea lions from different rookeries forage in different locations, or if they take different types of prey, then isotopic values should differ among sea lion rookeries. One weakness of the isotopic approach is that dietary composition can only be determined at a coarse level (Holst et al. 2001). 556 MARINE MAMMAL SCIENCE, VOL. 24, NO. 3, 2008 Figure 1. Location of California sea lion rookeries where fur and scat samples were collected: 1. Los Islotes (24◦35N, 110◦23W); 2. Farallon´ de San Ignacio (25◦26N, 109◦22W); 3. San Pedro Nolasco (26◦49N, 121◦12W); 4. San Pedro Martir´ (28◦24N, 112◦25W); 5. San Esteban (28◦42N, 112◦36W); 6. El Rasito (28◦49N, 112◦59W); 7. El Partido (28◦53N, 113◦02W); 8. Los Machos (29◦20N, 113◦30W); 9. Los Cantiles (29◦32N, 113◦29W); 10. Isla Granito (29◦34N, 113◦32W); 11. Isla Lobos (30◦02N, 114◦28W); 12. San Jorge (31◦01N, 113◦15W); 13. Rocas Consag (31◦7N, 114◦30W). The Midriff Region is indi- cated by dash lines. In our study we remedy this shortcoming by applying both stable isotope and scat analyses to establish the spatial structure of the sea lion foraging throughout the Gulf of California and to assess the trophic level and potential trophic overlap among sea lions at different rookeries. PORRAS-PETERS ET AL.: CALIFORNIA SEA LIONS 557 METHODS Fur and scat samples were collected at different California sea lion rookeries in the Gulf of California, Mexico (Fig. 1). A total of 188 fur samples from sea lion pups were collected at 13 rookeries, primarily during the breeding seasons of 2000 (16–25 July) and 2002 (15–31 July), with a small sample from 2004 (9–22 July). Fur was clipped with scissors at the base from an area of approximately 5 × 5 cm on the middorsal region. In our study, we analyzed fur from suckling California sea lion pups (approximately 2-mo old), assuming that they would accurately record differences in the foraging patterns in their mothers (see Aurioles-Gamboa et al. 2006 for a similar applica- tion). To interpret maternal dietary patterns from pup fur, the isotopic fractionations associated with mother-to-offspring nutrient transfer during pregnancy, lactation, and weaning must be known. Unfortunately, these fractionations are still poorly un- derstood. Theoretically, if milk protein has a nitrogen isotope value similar to other maternal tissues, then suckling offspring should have 15N-enriched values indicating that they are feeding one trophic level higher than their mother. This expected pattern has been observed in a number of species, including California sea lions (Newsome et al. 2006). Because of the smaller magnitude of trophic level 13C-enrichment, and the fact that milk is rich in 13C-depleted lipids, the fractionation from mother to suckling infant is difficult to predict a priori, and appears to be negative in pinnipeds (Newsome et al. 2006). Here, we provide further constraints on these fractionations through a comparison of isotope values for fur between adult females and suckling pups at one rookery. The fur samples from eight adult females were collected from the Los Islotes rookery in April 2003. We did not attempt to match mother-pup pairs, and we recognize that the fur sampled from adult females likely formed after the 2002 breeding season. However, given the difficulty of capturing adult females, it was not possible to sample them in previous seasons or at other rookeries. Scat samples were collected from 11 rookeries during the breeding season of 2002 (15–31 July). Most of the scat samples were from mothers with pups, as we were collecting at breeding areas dominated by adult females. Stable Isotope Analysis Fur samples were rinsed with distilled water and then fully dried at 80◦C for approximately 12 h. Lipids were removed using the Microwave Assisted Extraction (MAE) protocol (microwave oven model 1,000 MARS 5 x CEM) with 25 mL of a (1:1) solution of chloroform/methanol (Bligh and Dyer 1959). Samples were subsequently dried and ground into a homogeneous fine powder.
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