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Assessing Feeding Preferences of a Consumer Guild: Partitioning Variation Among Versus Within Species

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Assessing Feeding Preferences of a Consumer Guild: Partitioning Variation Among Versus Within Species vol. 192, no. 3 the american naturalist september 2018 Assessing Feeding Preferences of a Consumer Guild: Partitioning Variation Among versus Within Species O. Kennedy Rhoades,1,* Rebecca J. Best,2 and John J. Stachowicz3 1. Bodega Marine Laboratory, University of California, Davis, Bodega Bay, California 94923; and Smithsonian National Museum of Natural History, Smithsonian Marine Station at Fort Pierce, Florida 34949; 2. School of Earth Sciences and Environmental Sustainability, Northern Arizona University, Flagstaff, Arizona 86011; 3. Department of Evolution and Ecology, University of California, Davis, California 95616 Submitted September 1, 2017; Accepted March 1, 2018; Electronically published July 20, 2018 Online enhancements: supplemental material. Dryad data: http://dx.doi.org/10.5061/dryad.5nq06fj. abstract: Interspecific variation in resource use is critical to un- predicts population persistence (Werner et al. 1983), species derstanding species diversity, coexistence, and ecosystem functioning. interactions (Sommer et al. 2001; Burkepile and Hay 2008; A growing body of research describes analogous intraspecific varia- Rasher et al. 2013), species coexistence (Chesson 2000), and tion and its potential importance for population dynamics and com- community assembly (Grant and Grant 2006). Similarly, a munity outcomes. However, the magnitude of intraspecific variation rel- growing body of work indicates that individuals within species ative to interspecific variation in key dimensions of consumer-resource consistently vary in their resource use (Bolnick et al. 2003; Sih interactions remains unknown, hampering our understanding of the im- et al. 2004a; Vellend and Geber 2005). Individual variation in portance of this variation for population and community processes. In fl this study, we examine feeding preference through repeated laboratory resource use in uences population persistence (Hughes and choice feeding assays of 444 wild-caught individuals of eight invertebrate Stachowicz 2011; Forsman and Wennersten 2016), ecological grazer species on rocky reefs in northern California. Between-species var- processes and community structure (Crutsinger et al. 2006; iation accounted for 25%–33% of the total variation in preference for the Hughes et al. 2008), community assembly (Jung et al. 2010; preferred resource, while between-individual variation accounted for 4%– Siefert 2012; Kraft et al. 2014), community stability (Agashe 5% of total variation. For two of the eight species, between-individual var- 2009; Pruitt et al. 2016; Wood et al. 2017), species coexistence fi iation was signi cantly different from zero and on average contributed 14% (Vellend 2006; Lichstein et al. 2007; Lankau 2009), and food and 17% of the total diet variation, even after accounting for differences due to size and sex. Therefore, even with clearly distinguishable between- web structure (Barbour et al. 2016).Yet itisoften assumedthat species differences in mean preference, diet variation between and within phenotypic variation among individuals is negligible com- individuals can contribute to the dietary niche width of species and guilds, pared with that among species (Lister 1976; Taper and Case which may be overlooked by focusing solely on species’ mean resource 1985; Schoener 1986; McGill et al. 2006; Petchey and Gaston use patterns. 2006). This assumption may be premature, given the limited fi fi number of empiricalassessments of intraspeci c diversity that Keywords: intraspeci c variation, feeding preference, dietary niche, fi herbivory, rocky shore, kelp forest. quantify the relative proportion of intraspeci c versus inter- specific variation in resource use across an entire guild (Bol- nick et al. 2011; Siefert 2012; Kamath and Losos 2017). Also, Introduction existing assessments of individual specialization are likely biasedinfavorofspeciesknowntohaveconsiderableintraspe- Population dynamics and community structure are strongly cific variation, which may overestimate the general nature of influenced by the degree to which individuals and species spe- these effects (Bolnick et al. 2003). Although plant ecologists cialize on and partition available resources (Macarthur and have made significant progress in assessing the proportion of Levins 1967). Species vary broadly in their resource use within trait variation among and within species (Siefert et al. 2015), communities (Schoener 1974), and resource partitioning we have much less understanding of how these different levels of variation matter for species interactions, especially across trophic levels. * Corresponding author; email: [email protected]. In contrast with many other ecological traits (e.g., indirect ORCIDs: Rhoades, http://orcid.org/0000-0003-1456-1581; Best, http://orcid proxies of resource use, such as morphology and physiology), .org/0000-0003-2103-064X; Stachowicz, http://orcid.org/0000-0003-2735-0564. diet is a direct measure of consumer resource use for popula- Am. Nat. 2018. Vol. 192, pp. 000–000. q 2018 by The University of Chicago. 0003-0147/2018/19203-57924$15.00. All rights reserved. tions and species that also impacts the coexistence of compet- DOI: 10.1086/698325 itors and trophic interactions. Dietary niche width consists of This content downloaded from 169.237.066.128 on August 01, 2018 09:36:51 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 000 The American Naturalist a between-individual component (BIC) and a within-individual largely through short-term laboratory experiments and field- component (WIC; Roughgarden 1972). In addition to predict- tracking surveys, which cannot assess consistent variation able between-individual variation due to size (Werner and among individuals in preference or variation in a single indi- Gilliam 1984), age (Polis 1984), and sex (Shine 1989), a broad vidual’s preference over time (Chapman 2000). range of taxa exhibit consistent between-individual differ- To address this knowledge gap, we repeatedly measured ences in diet that are not attributable to these characteristics the feeding preference of 444 individual herbivores of eight (Bolnick et al. 2003; Sih et al. 2004a). Indeed, some individuals species using a suite of generally available algal foods to es- may be specialists that each consume only a narrow range of timate the relative magnitude of interspecific and intraspe- the resources consumed by the population (Bolnick et al. cificdietvariation.Specifically, we asked two questions. First, 2003; Tinker et al. 2008; Woo et al. 2008; Kernaleguen et al. what is the relative magnitude of interspecific versus intraspe- 2015), whereas others are individual generalists that each cific variation in feeding preference? Second, is individual var- consume the full range of resources consumed by the popula- iation in preference within species primarily due to consistent tion (Costa et al. 2015). Individual specialization is fairly com- specialization among individuals (BIC) or generalist variation mon and BIC is large for some taxa, but the relative magni- within individuals (WIC)? We interpret our results in light of tude of BIC and WIC in contributing to dietary niche width how species that share similar feeding preference differ in the across entire consumer assemblages has rarely been quanti- magnitude and source of individual variation (within vs. be- fied (Bolnick et al. 2011; Maldonado et al. 2017). tween individuals), potentially exerting different structuring Individual dietary specialization can arise from differences influence on prey assemblages. in morphology, physiology or behavior, or genotype (Bolnick et al. 2003, 2011). Of these mechanisms, feeding behaviors are easily comparable across diverse taxa and trophic levels Methods and are the most proximate measures of diet. Moreover, var- iation in feeding preference (West 1988; Estes et al. 2003), We collected animals and algae from rocky reef habitats be- habitat use (Werner 1977; Matthews et al. 2010), and activity tween Bodega Bay (38.3332507N, 123.0480577W) and Point level (Pruitt et al. 2012, 2017) can produce interindividual var- Arena Cove (38.9140767N, 123.7089077W) in northern Cali- iation in the size, type, and traits of prey obtained by con- fornia. Among a diverse community of herbivorous mollusks, sumers. Furthermore, variation in these behaviors is closely crustaceans, and echinoderms on northern California rocky tied to and has clear implications for ecological processes and shores, we selected the most common, mobile invertebrate ecosystem dynamics; individual variation in feeding behavior macrograzers occurring in the intertidal and shallow subtidal directly impacts key ecological processes, such as top-down zones. These species included Mesocentrotus (formerly Stron- control (Belgrad and Griffen 2016; Michalko and Pekar 2017; gylocentrotus) franciscanus (red urchin, n p 27), Strongylo- Pruitt et al. 2017), interspecific competition, and coexistence centrotus purpuratus (purple urchin, n p 37), Haliotis ru- (Gibert and Brassil 2014; Hart et al. 2016). We therefore focus fescens (red abalone, n p 36), Tegula brunnea (brown on feeding behavior—specifically, feeding preference—as the turban snail, n p 79), Pugettia producta (northern kelp crab, proxy for the dietary niche and ecological function. n p 50), Pagurus samuelis (blueband hermit crab, n p 79), California kelp forests and adjacent rocky shores support Pachygrapsus crassipes (lined shore crab, n p 49), and Tegula complex food webs that host diverse
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