Farallon Institute Technical Report

Temporal Variation in California Food Habits: 2010 and 2013

Jason Hassrick1, Heather Robinson1, Keith Hernandez2, Patricia Morris1, Julie Thayer1, and Michael Weise3

1 Farallon Institute, 101 H St., Suite Q, Petaluma, CA, 94952

2 Moss Landing Marine Laboratory, 8272 Moss Landing Rd, Moss Landing, CA 95039

3 Office of Naval Research, One Liberty Center, 875 N. Randolph St., Arlington, VA 22203-1995

Introduction Physical dynamics of the marine environment affect distribution and abundance of prey resources and in turn influence the distribution and foraging behavior of top predators (Sydeman et al. 2013). The relationships among marine conditions and food webs are difficult to study, but insights can be gained from examining changes in top predators because they integrate processes over multiple temporal scales and trophic levels (Block et al. 2002). In particular, dietary studies of top predators may be used to infer abundance and structure of food webs and contribute to understanding how physical processes affect the dynamics of forage species. Moreover, through bioenergetics models that use a combination of diet composition and prey energetic resources, one can also estimate predator impacts on commercially-valuable populations (Weise and Harvey 2008). Because they breed on land, diets of seabirds and pinnipeds are commonly studied by analysis of undigested hard parts of prey that remain in pellets or scats, the sampling of which does not require handling and is minimally invasive in comparison to other techniques (e.g., dissection, stomach lavage, enema, or tissue sampling for stable isotopes or fatty acids). The California Current Ecosystem (CCE) is one of the large upwelling ecosystems in the world. Upwelling in this eastern boundary current varies both temporally and spatially, but the CCE is also subject to long-term oceanographic oscillations in response to El Niño and La Niña cycles and the Pacific Decadal Oscillation (PDO) (Bograd and Lynn 2001; Peterson and Schwing 2003). These dynamics influence the distribution and abundance of organisms throughout the CCE (Brodeur et al. 2006; Block et al. 2011). California sea lions (Zalophus californianus, hereafter CSL) are ubiquitous in the CCE, with an estimated population size of a 250,000 individuals in US waters, growing at a rate of >5% per year since the passage of the Marine Mammal Protection Act in 1972 (Carretta et al. 2005). California sea lions feed on a variety of fish and squid species (Lowry 2011). As such, their diets may be an indicator of food web characteristics in the CCE (Weise and Harvey 2008). The purpose of this study is to characterize the diet of CSL sampled at a single site, Año Nuevo Island, and compare their food habits in 2010 and 2013. This is part of a long term study that is evaluating changes in food habits and demography of the species in response to climate and ocean variability.

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Materials and Methods Located off the central California coast, Año Nuevo Island (ANI; 37.108°N, 122.336°W) rises 9 m above sea level and sits 650 m offshore of Point Año Nuevo, San Mateo County, CA (Fig 1.). Fecal samples were collected on a weekly basis from CSL colonies located around the island from March through December of 2010 and from July to September of 2013. Samples were frozen and stored for processing at Moss Landing Marine Laboratories (MLML). Scat samples were processed using a washing machine and sieves following Orr et al. (2003) and identified using reference photographs (Lowry 2011) and collections of otoliths at MLML (Harvey 1987; Weise and Harvey 2005). Squid beaks have not been enumerated in our analysis due to a shortage of funding to support the identification process, but they were collected for future incorporation.

Results / Discussion Prey in sea lion scats were significantly more diverse (F1, 201 = 27.7, p < 0.0001; Table 1) in 2010 than in 2013. Estimates of frequency of occurrence (FO) indicate that Pacific hake (Merluccius productus) was the predominant prey item in both years (36% and 61% FO respectively), followed by rockfish (Sebastes sp.) (Table 2). Northern anchovy (Engraulis mordax) was more equally represented in both years, with 12% FO in 2010 and 8% in 2013. Pacific sardine (Sardinops sagax) was more abundant in 2010 when they comprised 22% FO relative to 2% in 2013 when they were virtually absent. Although it is possible that the difference in sampling diversity could be due to temporal differences in the sampling window between the two years (see Table 1), remotely-sensed satellite imagery of monthly averaged chlorophyll-a with a midpoint on July 16 (Fig. 4) suggests that greater phytoplankton biomass in 2010 may correspond to the apparent greater abundance and diversity of prey in sea lion scats in that year.

Conclusion In a previous study of California sea lion diet at ANI conducted between 1997 and 1999, Weise and Harvey (2008) reported Pacific sardine and market squid (Loligo opalescens) as the most abundant species, followed by northern anchovy, rockfish, and Pacific hake. The relative scarcity of Pacific sardine in 2010 and, in particular, 2013, along with abundance of Pacific hake and anchovy in the diet indicates a change in coastal food web structure has taken place over these years. The findings of this study, in contrast to previous findings in the late 1990s, highlight the potential for long time series diet studies to contribute to our understanding of food web dynamics in the California Current. The years 1997-1998 and 2009-2010 were both characterized by El Niño conditions, with apparently different food web structures. Funding for future work should include analysis of scat samples collected in years prior to 2013, and continued effort to collect samples and expand the time series.

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Figure 1. A satellite image of Año Nuevo Island (37.108°N, 122.336°W). The dark area marked with box represents an area on the island where sea lions are excluded by fencing; scat samples were not collected in this area.

Table 1. California sea lion prey sampling in 2010 and 2013. Days refer to the number of days samples were collected on the island.

Year Days Samples Total Otoliths No. Prey Species

2010 33 (25 Feb – 31 Dec) 116 2770 29 2013 15 (05 Jul – 28 Aug) 86 1040 16

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Table 2. The percent frequency of occurrence (%FO) and percent by number (%Number) for forage fish in California sea lion diet samples collected in 2010 and 2013. Cephalopods were present in the diet, but were not analyzed for this table.

2010 2013 Prey %FO %Number %FO %Number Allosmerus elongatus 0.86 0.07 Chilara taylori 1.16 0.34 Citharichthys sordidus 11.21 2.56 11.63 2.05 Citharichthys stigmaeus 5.17 1.37 1.16 0.20 Clupea pallisii 5.17 1.40 3.49 1.97 Cololabis saira 7.76 3.08 1.16 0.04 Cottidae 12.07 2.37 3.49 1.45 Cymatogaster aggregata 9.48 4.14 2.33 0.10 Diaphus theta 0.86 0.03 Embiotocidae 1.72 0.77 Engraulis mordax 12.07 3.09 8.14 4.15 Genyonemus lineatus 8.62 1.77 4.65 0.51 Glyptocephalus zachirus 5.17 0.80 3.49 0.44 Hyperprosopon anale 0.86 0.52 Icelinus filamentosus 0.86 1.03 Icichtys lockingtoni 1.72 0.37 Leptocottus armatus 7.76 2.82 Leuroglossus stilbius 0.86 0.01 Lyopsetta exilis 5.17 1.26 Merluccius productus 36.21 21.41 61.63 49.16 Microstomus pacificus 11.21 3.20 Orthonopias triacis 0.86 0.02 Parophrys vetulus 3.45 0.21 1.16 0.46 Pleuronectidae 10.34 2.15 2.33 0.70 Porichthys notatus 3.45 0.26 Sardinops sagax 22.41 16.99 2.33 0.29 Sebastes sp. 41.38 24.31 53.49 36.78 Stenobrachius leucopsarus 9.48 2.10 1.16 1.37 Symbolophorus californiensis 0.86 0.15 Tarletonbenia crenularis 4.31 1.71

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Figure 2. Grid data of chlorophyll-a (mg m-3) from Aqua MODIS, NPP, at 0.025 degrees. 2010 (left), 2013 (right). Warmer colors indicate higher chlorophyll-a concentrations. (Data courtesy of NASA GSFC (OBPG)). Acknowledgements Research was conducted under ethical care and use guidelines approved by San Jose State University’s IACUC. This project was conducted under National Marine Fisheries Service permit #17952 with funding from the Office of Naval Research award # N00014-13-1-0377. Bill Sydeman and Sarah Ann Thompson provided insightful reviews. We thank Dan Crocker and Stephanie Thebault at Sonoma State University for use of their laboratory and Jim Harvey at Moss Landing Marine Labs for of his wet lab. We are also grateful to Bonnie Brown for assistance with scat processing and Año Nuevo Island Reserve for granting access to the field site.

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Brodeur RD, Ralston S, Emmett RL, Trudel M, Auth TD, Phillips AJ (2006) Anomalous pelagic nekton abundance, distribution, and apparent recruitment in the northern California Current in 2004 and 2005. Geophysical Research Letters 33: L22S08 Carretta JV, Forney KA, Muto MM, Barlow J, Baker J, Hansen B, Lowry MS (2005) U.S. marine mammal stock assessments: 2004. NOAA Tech Memo, NOAA-TM-NMFS-SWFSC-375. Available from SWFSC, 8604 La Jolla Shores Drive, La Jolla, California 92037. Harvey JT (1987) Population dynamics, annual food consumption, movements, and dive behaviors of harbor seals, Phoca vitulina richardis, in Oregon. Doctoral Dissertation Lowry MS (2011) Photographic catalog of California marine fish otoliths: prey of California sea lions (Zalophus californianus). In: Division PR (ed). Southwest Fisheries Science Center, La Jolla, California Orr AJ, Laake JL, Dhruv MI, Banks AS, DeLong RL, Huber HR (2003) Comparison of processing pinniped scat samples using a washing machine and nested sieves. Wildlife Society Bulletin 31: 253-257 doi 10.2307/3784381 Peterson WT, Schwing FB (2003) A new climate regime in northeast Pacific ecosystems. Geophysical Research Letters 30: 1896 Sydeman WJ, Santora JA, Thompson SA, Marinovic B, Lorenzo ED (2013) Increasing variance in North Pacific climate relates to unprecedented ecosystem variability off California. Global Change Biology 19: 1662-1675 doi 10.1111/gcb.12165 Weise MJ, Harvey JT (2005) Impact of the California sea lion (Zalophus californianus) on salmon fisheries in Monterey Bay, California. Fishery Bulletin 103: 685-696 Weise MJ, Harvey JT (2008) Temporal variability in ocean climate and California sea lion diet and biomass consumption: implications for fisheries management. Marine Ecology- Progress Series 373: 157-172

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