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Open Access Publications from the University of California

Scholarly Works (9 results)

  • Thesis
  • Peer Reviewed
UC Santa Cruz Electronic Theses and Dissertations (2016)

Foraging behavior is a key ecological factor that has wide-ranging implications for individual fitness, and population and ecosystem dynamics. There are multiple hierarchical levels at which foraging behavior can be studied, from broad descriptions at the species level to the lowest level of within-individual variability. Intraspecific variation in foraging behavior is increasingly recognized as both widespread and ecologically important, and the occurrence and consistency of individual variation in foraging behavior has implications for the ability of populations to adapt to environmental change. The focus of my dissertation is on quantifying inter- and intra-individual variability in foraging behavior and the energetic implications of these differences for California sea lions (Zalophus californianus), an abundant generalist predator that inhabits a dynamic ecosystem. The fine- and broad-scale foraging behavior of adult female sea lions was quantified at multiple temporal scales using bio-logging technology and stable isotope analysis. Concurrent measurements of foraging behavior and energy expenditure were used to determine the energetic implications of behavioral variability. I found that female California sea lions used three foraging strategies: a shallow epipelagic strategy, a mixed epipelagic/benthic strategy, and a deep-diving strategy. This diversity in foraging behavior has likely allowed them to be successful in such a dynamic ecosystem, as I found evidence that female sea lions switched foraging strategies in response to changes prey availability. Despite this apparent flexibility, females generally exhibited behavioral consistency across both short and long time scales, including periods of reduced prey availability. Collectively, these results indicate that female California sea lions likely do switch foraging strategies, but it is unlikely that most sea lions routinely use all three strategies. Instead, they largely appear to play it safe by consistently using similar habitats and/or dive behaviors, which may be a successful strategy for managing uncertainty in environmental conditions. These individual behavioral differences have implications for survival and fitness, as fine-scale behavior affected the rate of energy expenditure. My dissertation highlights the importance of quantifying inter- and intra-individual variation in foraging behavior, particularly as it relates to understanding the strategies that individuals and species use to cope with limited prey resources in dynamic environments.

    Cover page: An individual-based approach to the foraging behavior and energetics of a generalist marine predator
    • Article
    • Peer Reviewed
    UC Santa Cruz Previously Published Works (2019)
    Quantifying metabolic rates and the factors that influence them is key to wildlife conservation efforts because anthropogenic activities and habitat alteration can disrupt energy balance, which is critical for reproduction and survival. We investigated the effect of diving behaviour, diet and season on field metabolic rates (FMR) and foraging success of lactating northern fur seals (Callorhinus ursinus) from the Pribilof Islands during a period of population decline. Variation in at-sea FMR was in part explained by season and trip duration, with values that ranged from 5.18 to 9.68 W kg-1 (n = 48). Fur seals experienced a 7.2% increase in at-sea FMR from summer to fall and a 1.9% decrease in at-sea FMR for each additional day spent at sea. There was no effect of foraging effort, dive depth or diet on at-sea FMR. Mass gains increased with trip duration and were greater in the fall compared with summer, but were unrelated to at-sea FMR, diving behaviour and diet. Seasonal increases in at-sea FMR may have been due to costs associated with the annual molt but did not appear to adversely impact the ability of females to gain mass on foraging trips. The overall high metabolic rates in conjunction with the lack of any diet-related effects on at-sea FMR suggests that northern fur seals may have reached a metabolic ceiling early in the population decline. This provides indirect evidence that food limitation may be contributing to the low pup growth rates observed in the Pribilof Islands, as a high metabolic overhead likely results in less available energy for lactation. The limited ability of female fur seals to cope with changes in prey availability through physiological mechanisms is particularly concerning given the recent and unprecedented environmental changes in the Bering Sea that are predicted to have ecosystem-level impacts.
      Cover page: Factors affecting energy expenditure in a declining fur seal population.
      • Article
      • Peer Reviewed
      UC Santa Cruz Previously Published Works (2016)

      Rationale

      Mixing models are a common method for quantifying the contribution of prey sources to the diet of an individual using stable isotope analysis; however, these models rely upon a known trophic discrimination factor (hereafter, TDF) that results from fractionation between prey and animal tissues. Quantifying TDFs in captive animals is ideal, because diet is controlled and the proportional contributions and isotopic values of all prey items are known.

      Methods

      To calculate TDFs for the Hawaiian monk seal, northern elephant seal, bearded seal, ringed seal, spotted seal, harbor seal, and California sea lion, we obtained whiskers, serum, plasma, red blood cells, and prey items from nine captive individuals. We obtained δ(13) C and δ(15) N values using continuous-flow isotope-ratio mass spectrometry. The average δ(13) C and δ(15) N values from bulk and lipid-corrected prey from the diet were subtracted from the δ(13) C and δ(15) N values of each blood and whisker sample to calculate tissue-specific TDFs for each individual (∆(13) C or ∆(15) N).

      Results

      The ∆(13) C values ranged from +1.7 to +3.2‰ (bulk prey) and from +0.8 to +1.9‰ (lipid-corrected prey) for the various blood components, and from +3.9 to +4.6‰ (bulk prey) or +2.6 to +3.9‰ (lipid-corrected prey) for whiskers. The ∆(15) N values ranged from +2.2 to +4.3‰ for blood components and from +2.6 to +4.0‰ for whiskers. The TDFs tended to group by tissue, with whiskers having greater ∆(13) C values than blood components. In contrast, the ∆(15) N values were greater in serum and plasma than in red blood cells and whiskers.

      Conclusions

      By providing the first TDF values for five seal species (family Phocidae) and one otariid species (family Otariidae), our study facilitates more accurate mixing models for these species. These values are particularly important for critically endangered Hawaiian monk seals and the three Arctic seal species (bearded, ringed, and spotted) that are faced with a rapidly changing environment.
        Cover page: Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species
        • Article
        • Peer Reviewed
        UC Santa Cruz Previously Published Works (2018)
        Intraspecific variability in foraging behavior has been documented across a range of taxonomic groups, yet the energetic consequences of this variation are not well understood for many species. Understanding the effect of behavioral variation on energy expenditure and acquisition is particularly crucial for mammalian carnivores because they have high energy requirements that place considerable pressure on prey populations. To determine the influence of behavior on energy expenditure and balance, we combined simultaneous measurements of at-sea field metabolic rate (FMR) and foraging behavior in a marine carnivore that exhibits intraspecific behavioral variation, the California sea lion (Zalophus californianus). Sea lions exhibited variability in at-sea FMR, with some individuals expending energy at a maximum of twice the rate of others. This variation was in part attributable to differences in diving behavior that may have been reflective of diet; however, this was only true for sea lions using a foraging strategy consisting of epipelagic (<200 m within the water column) and benthic dives. In contrast, sea lions that used a deep-diving foraging strategy all had similar values of at-sea FMR that were unrelated to diving behavior. Energy intake did not differ between foraging strategies and was unrelated to energy expenditure. Our findings suggest that energy expenditure in California sea lions may be influenced by interactions between diet and oxygen conservation strategies. There were no apparent energetic trade-offs between foraging strategies, although there was preliminary evidence that foraging strategies may differ in their variability in energy balance. The energetic consequences of behavioral variation may influence the reproductive success of female sea lions and result in differential impacts of individuals on prey populations. These findings highlight the importance of quantifying the relationships between energy expenditure and foraging behavior in other carnivores for studies addressing fundamental and applied physiological and ecological questions.
          Cover page: The energetic consequences of behavioral variation in a marine carnivore
          • Article
          • Peer Reviewed
          UC Santa Cruz Previously Published Works (2016)

          Rationale

          Mixing models are a common method for quantifying the contribution of prey sources to the diet of an individual using stable isotope analysis; however, these models rely upon a known trophic discrimination factor (hereafter, TDF) that results from fractionation between prey and animal tissues. Quantifying TDFs in captive animals is ideal, because diet is controlled and the proportional contributions and isotopic values of all prey items are known.

          Methods

          To calculate TDFs for the Hawaiian monk seal, northern elephant seal, bearded seal, ringed seal, spotted seal, harbor seal, and California sea lion, we obtained whiskers, serum, plasma, red blood cells, and prey items from nine captive individuals. We obtained δ(13) C and δ(15) N values using continuous-flow isotope-ratio mass spectrometry. The average δ(13) C and δ(15) N values from bulk and lipid-corrected prey from the diet were subtracted from the δ(13) C and δ(15) N values of each blood and whisker sample to calculate tissue-specific TDFs for each individual (∆(13) C or ∆(15) N).

          Results

          The ∆(13) C values ranged from +1.7 to +3.2‰ (bulk prey) and from +0.8 to +1.9‰ (lipid-corrected prey) for the various blood components, and from +3.9 to +4.6‰ (bulk prey) or +2.6 to +3.9‰ (lipid-corrected prey) for whiskers. The ∆(15) N values ranged from +2.2 to +4.3‰ for blood components and from +2.6 to +4.0‰ for whiskers. The TDFs tended to group by tissue, with whiskers having greater ∆(13) C values than blood components. In contrast, the ∆(15) N values were greater in serum and plasma than in red blood cells and whiskers.

          Conclusions

          By providing the first TDF values for five seal species (family Phocidae) and one otariid species (family Otariidae), our study facilitates more accurate mixing models for these species. These values are particularly important for critically endangered Hawaiian monk seals and the three Arctic seal species (bearded, ringed, and spotted) that are faced with a rapidly changing environment.
            Cover page: Seals and sea lions are what they eat, plus what? Determination of trophic discrimination factors for seven pinniped species
            • Article
            • Peer Reviewed
            UC Santa Cruz Previously Published Works (2023)
            Growth of structural mass and energy reserves influences individual survival, reproductive success, population and species life history. Metrics of structural growth and energy storage of individuals are often used to assess population health and reproductive potential, which can inform conservation. However, the energetic costs of tissue deposition for structural growth and energy stores and their prioritization within bioenergetic budgets are poorly documented. This is particularly true across marine mammal species as resources are accumulated at sea, limiting the ability to measure energy allocation and prioritization. We reviewed the literature on marine mammal growth to summarize growth patterns, explore their tissue compositions, assess the energetic costs of depositing these tissues and explore the tradeoffs associated with growth. Generally, marine mammals exhibit logarithmic growth. This means that the energetic costs related to growth and tissue deposition are high for early postnatal animals, but small compared to the total energy budget as animals get older. Growth patterns can also change in response to resource availability, habitat and other energy demands, such that they can serve as an indicator of individual and population health. Composition of tissues remained consistent with respect to protein and water content across species; however, there was a high degree of variability in the lipid content of both muscle (0.1-74.3%) and blubber (0.4-97.9%) due to the use of lipids as energy storage. We found that relatively few well-studied species dominate the literature, leaving data gaps for entire taxa, such as beaked whales. The purpose of this review was to identify such gaps, to inform future research priorities and to improve our understanding of how marine mammals grow and the associated energetic costs.
              Cover page: Growth in marine mammals: a review of growth patterns, composition and energy investment.
              • Article
              • Peer Reviewed
              UC Santa Cruz Previously Published Works (2024)
              Deep ocean foraging northern elephant seals (Mirounga angustirostris) consume fish and squid in remote depths of the North Pacific Ocean. Contaminants bioaccumulated from prey are subsequently transferred by adult females to pups during gestation and lactation, linking pups to mercury contamination in mesopelagic food webs (200-1000 m depths). Maternal transfer of mercury to developing seal pups was related to maternal mercury contamination and was strongly correlated with maternal foraging behavior (biotelemetry and isotopes). Mercury concentrations in lanugo (hair grown in utero) were among the highest observed worldwide for young pinnipeds (geometric mean 23.01 μg/g dw, range 8.03-63.09 μg/g dw; n = 373); thus, some pups may be at an elevated risk of sub-lethal adverse health effects. Fetal mercury exposure was affected by maternal foraging geographic location and depth; mercury concentrations were highest in pups of the deepest diving, pelagic females. Moreover, pup lanugo mercury concentrations were strongly repeatable among successive pups of individual females, demonstrating relative consistency in pup mercury exposure based on maternal foraging strategies. Northern elephant seals are biosentinels of a remote deep-sea ecosystem. Our results suggest that mercury within North Pacific mesopelagic food webs may also pose an elevated risk to other mesopelagic-foraging predators and their offspring.
                Cover page: Foraging behavior and age affect maternal transfer of mercury to northern elephant seal pups.
                • Article
                • Peer Reviewed
                UC Santa Cruz Previously Published Works (2018)
                Characterizing habitat suitability for a marine predator requires an understanding of the environmental heterogeneity and variability over the range in which a population moves during a particular life cycle. Female California sea lions (Zalophus californianus) are central-place foragers and are particularly constrained while provisioning their young. During this time, habitat selection is a function of prey availability and proximity to the rookery, which has important implications for reproductive and population success. We explore how lactating females may select habitat and respond to environmental variability over broad spatial and temporal scales within the California Current System. We combine near-real-time remotely sensed satellite oceanography, animal tracking data (n = 72) from November to February over multiple years (2003-2009) and Generalized Additive Mixed Models (GAMMs) to determine the probability of sea lion occurrence based on environmental covariates. Results indicate that sea lion presence is associated with cool (<14°C), productive waters, shallow depths, increased eddy activity, and positive sea-level anomalies. Predictive habitat maps generated from these biophysical associations suggest winter foraging areas are spatially consistent in the nearshore and offshore environments, except during the 2004-2005 winter, which coincided with an El Niño event. Here, we show how a species distribution model can provide broadscale information on the distribution of female California sea lions during an important life history stage and its implications for population dynamics and spatial management.
                  Cover page: Characterizing habitat suitability for a central-place forager in a dynamic marine environment.
                  • Article
                  • Peer Reviewed
                  UC Santa Cruz Previously Published Works (2023)
                  Forage fishes are key energy conduits that transfer primary and secondary productivity to higher trophic levels. As novel environmental conditions caused by climate change alter ecosystems and predator-prey dynamics, there is a critical need to understand how forage fish control bottom-up forcing of food web dynamics. In the northeast Pacific, northern anchovy (Engraulis mordax) is an important forage species with high interannual variability in population size that subsequently impacts the foraging and reproductive ecology of marine predators. Anchovy habitat suitability from a species distribution model (SDM) was assessed as an indicator of the diet, distribution and reproduction of four predator species. Across 22 years (1998-2019), this anchovy ecosystem indicator (AEI) was significantly positively correlated with diet composition of all species and the distribution of common murres (Uria aalge), Brandts cormorants (Phalacrocorax penicillatus) and California sea lions (Zalophus californianus), but not rhinoceros auklets (Cerorhinca monocerata). The capacity for the AEI to explain variability in predator reproduction varied by species but was strongest with cormorants and sea lions. The AEI demonstrates the utility of forage SDMs in creating ecosystem indicators to guide ecosystem-based management.
                    Cover page: An anchovy ecosystem indicator of marine predator foraging and reproduction.
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