1. Introduction
Predator-prey relations are an integral force in many communities and are often key to understanding how communities function. Predators occupy a wide spectrum of foraging strategies, ranging from generalists to specialists. Individuals using a smaller subset of resources than the population as a whole are defined as individual specialists (Van Valen, 1965) whereas individuals consuming a wider range of resources than used on average by the population are defined as generalists (Hanski, Hansson, & Henttonen, 1991). In some cases, preying on one species may preclude consumption of a different species as there may be trade-offs in skills required to utilize different resources (Arthur et al. 2016; Wilson & Yoshimura 1994). Inter-individual differences in resource use that are transient and the result of short-term choices in habitat or hunting strategies are best described as intrapopulation feeding diversity while permanent differences between individuals based on sex, size, or personality are better described as individual specialization (Van Valen 1965). Both types of inter-individual differences in resource use need to be examined to understand predator-prey interactions.
The level of individual specialization and/or intrapopulation feeding diversity can affect food web dynamics, responses to changes in prey availability, and the accuracy of predictive models (Bolnick et al., 2003). For example, in a population of bluegill sunfish Lepomis macrochirus prior experience foraging on a single prey type increases the likelihood of an individual using that resource, even when another resource becomes more profitable (Werner, Mittelbach, & Hall,1981). Further, theoretical models predict that changes in prey abundance in a system with highly specialized individuals (i.e. slow to switch preferred prey) are much more likely to have chaotic dynamics (Abrams & Matsuda, 2004). In general, dynamics can be sensitive to small variations in the speed of predators changing prey preferences (Abrams & Matsuda, 2004), which would be affected by the predator’s level of specialization. More generally, diversification within a population can have significant impacts on ecosystems functions, such as prey community structure (Harmon et al., 2009). In addition, differences in a single species’ population structure can have larger impacts on community composition than differences between species (Rudolf & Rasmussen, 2013). These findings imply that differences between individuals of the same species can be important drivers of ecosystem functions (Harmon et al., 2009, Rudolf & Rasmussen, 2013). Thus, including metrics of variation in foraging decisions between individuals of the same population in ecosystem studies provides a more clear and accurate description of the system and ignoring them can be an oversimplification of the ecological interactions in the community (Araújo, Bolnick, & Layman, 2011; Bolnick et al., 2003; Bolnick et al., 2011; Dall, Bell, Bolnick, & Ratnieks, 2012). Unfortunately, most foraging studies do not describe the level of intraspecific variation in the predator population.
Variation in foraging decisions within populations of predators is difficult to describe empirically because they require observing a large number of predation events in multiple individuals across many ecological contexts. The empirical problems are even greater when studying predators that forage in environments where it is difficult to directly observe predation events (e.g., marine environments) and that prey on a large diversity of taxonomically similar prey species that make it difficult to determine which species has been consumed. Here, we demonstrate how the application of an individual diet specialization metric to a large set of molecular prey barcoding data from scat can be used to describe intrapopulation feeding diversity by examining the short-term variation in individual foraging decisions in a marine predator. Our analysis allowed us to explore 1) correlations of individual diet diversity with the sex of the predator and time of year in which the predation occurred, and 2) to test whether short-term diet diversity was related to the consumption of particular prey species and their preferred habitat.
Harbor seals (Phoca vitulina , Linnaeus 1758) have the largest worldwide distribution of any pinniped in coastal areas (Teilmann & Galatius, 2018) and appear to have reached carrying capacity in the Salish Sea (Jeffries, Huber, Calambokidis, & Laake, 2003; Olesiuk, 2009). Because harbor seals are abundant in the ecosystem and feed on a wide range of species, they have significant impacts on prey populations (Howard, Lance, Jeffries, & Acevedo-Gutiérrez, 2013; Lance, Chang, Jeffries, Pearson, & Acevedo-Gutiérrez, 2012; Olesiuk, Bigg, Ellis, Crockford, & Wigen, 1990). Some of their prey species are of high conservation concern, such as Pacific salmon Oncorhynchus spp., rockfish Sebastes spp., and Pacific herring (Clupea pallasii pallasii, Valenciennes, 1847) (Bjorland et al., 2015; Bromaghin et al., 2013; Lance et al., 2012). . Harbor seal’s effect onOncorhynchus spp. is also of interest because they eat both juvenile and adult individuals (Thomas, Nelson, Lance, Deagle, & Trites, 2017). Eating juveniles may have considerable impacts on populations of Chinook (Oncorhynchus tshawytscha, Walbaum 1792), coho (Oncorhynchus kisutch, Walbaum 1792), and steelhead (Oncorhynchus mykiss, Walbaum 1792), as survival during the first several months at sea is believed to be the primary factor limiting population abundance and productivity (Beamish et al., 2010; Kendall, Marston, & Klungle, 2017; Neville, Beamish, & Chittenden, 2015).
Due to the large diversity of prey species that harbor seal populations eat, the species has historically been considered a generalist predator (Teilmann & Galatius, 2018). However, prey composition and foraging dive behavior of harbor seals in the Salish Sea vary relative to habitat, sex, and time of year (Lance et al., 2012; Olesiuk et al., 1990; Wilson, Lance, Jeffries, & Acevedo-Gutiérrez, 2014). Harbor seals also eat different types of prey depending on the type of environment in which they forage. Scat samples from haul-outs located in estuaries have higher prey diversity than those coming from outside estuaries (Lance et al., 2012; Luxa & Acevedo-Gutiérrez, 2013). Further, males and females consume different prey (Bjorland et al., 2015; Schwarz et al., 2018) and have different foraging dive patterns (Wilson et al., 2014). Specifically, females frequently perform longer and deeper foraging dives than males, and more commonly consume benthic species (Schwarz et al., 2018; Wilson et al., 2014).
These traits of high abundance and differences in diet and foraging patterns between males and females, suggest that harbor seals could display intrapopulation feeding diversity.. As such, ecosystem dynamics with regard to the effect of harbor seals on prey species are likely more complex than described in current models of the system which assume consistent generalized behavior (e.g. Chasco et al. 2017, Howard et al. 2013). As harbor seals are the most abundant mammalian predator in the Salish Sea, and prey on many species of economic and conservation concern, an accurate understanding of their role in ecosystem dynamics is important, for which high quality diet data are required. While current bioenergetics based models are useful descriptors of harbor seal consumption (e.g. Chasco et al. 2017, Howard et al. 2013), they can be improved by including the effects of different foraging strategies across sexes and individuals.
Obtaining high quality diet data from large, mobile organisms, such as marine mammals, can be costly and time consuming (Rothstein, McLaughlin, Acevedo-Gutiérrez, & Schwarz, 2017). Analysis of prey contents in scat via metabarcoding is a relatively cheap, non-invasive, and time efficient way to obtain large sample sizes with species-level taxonomic resolution (Deagle et al., 2005; Deagle et al., 2019; Rothstein et al., 2017; Tollit et al., 2009). However, to our knowledge, these molecular techniques have not previously been used to quantify intrapopulation feeding diversity at large spatial and temporal scales.
Here, we use molecular barcoding of prey DNA from scat in a novel way to examine intrapopulation feeding diversity, in harbor seals by answering the following questions: 1. How do the factors Sex, Time of year, Location, and Year affect cross sectional estimation of a specialization metric? 2. What prey items correlate with high levels of specialization relative to sex and environment? To answer these questions, we collected and analyzed scat from wild harbor seals in the Salish Sea. Diet of harbor seals was determined from the scat using both molecular and traditional techniques. Sex of the depositor was determined using molecular techniques. Diet data were analyzed with a proportional similarity index (Bolnick, Yang, Fordyce, Davis, & Svanbäck, 2002) to describe the variation in individual foraging decisions in harbor seals.