Intraspecific Behavioral Variation Mediates Insect Prey Survival Via

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Intraspecific Behavioral Variation Mediates Insect Prey Survival Via diversity Article Intraspecific Behavioral Variation Mediates Insect Prey Survival via Direct and Indirect Effects Benjamin J. Toscano 1,*, James L. L. Lichtenstein 2 and Raul Costa-Pereira 3 1 Department of Biology, Trinity College, Hartford, CT 06106, USA 2 Department of Ecology, Evolution and Marine Biology, University of California Santa Barbara, Santa Barbara, CA 93107, USA; [email protected] 3 Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas 13083-862, Brazil; [email protected] * Correspondence: [email protected] Received: 27 March 2020; Accepted: 12 April 2020; Published: 16 April 2020 Abstract: Conspecific individuals often exhibit behavioral differences that influence susceptibility to predation. Yet, how such trait differences scale to affect prey population regulation and community structure remains unclear. We used an 8 day field mesocosm experiment to explore the effects of intraspecific prey behavioral trait variation on survival in an herbivorous insect community. We further manipulated spider predator composition to test for top-down context-dependence of behavioral effects. Insect prey behavioral trait variance influenced survival through both direct (i.e., variation among conspecifics) and indirect (i.e., variation among heterospecifics) mechanisms. The behavioral variance of two prey species, Philaenus and Orchelimum, directly reduced their survival, though for Philaenus, this direct negative effect only occurred in the presence of a single spider predator species. In contrast, the survival of Scudderia was enhanced by the behavioral trait variance of the surrounding insect community, an indirect positive effect. Taken together, these results emphasize the importance of accounting for intraspecific variation in community ecology, demonstrating novel pathways by which individual-level behavioral differences scale to alter population and community level patterns. Keywords: animal personality; boldness; food web; herbivorous insects; indirect interaction; intraspecific trait variation; jumping spiders; old field; predator selection; trait-mediated 1. Introduction The importance of prey traits for predatory interactions spans multiple biological scales. For example, predators exert selection on prey populations by preferentially consuming individuals with certain trait values [1–6], but also modify community structure by disproportionally consuming one prey species over another [7]. This latter effect is often ascribed to mean, species-level trait differences [8–10]. Yet these classic empirical approaches overlook the ecological effects of trait variance within prey populations, an outcome of trait differences among individuals that can vary independently from trait means [11,12]. While it is unlikely that a single prey individual’s traits will modify outcomes at higher organizational scales (but see [13]), population-level prey trait variance could be an important property linking individual traits to the community-level effects of predators. Yet, few studies to date have experimentally explored the effects of prey trait variance on food webs [14–16]. Here, we used a field experiment to examine the effects of insect prey behavioral trait means and behavioral trait variances on the community-structuring effects of their predators (spiders). Prey trait variance directly impacts prey survival. For example, size-selective predators often have an optimal prey body size for which predation rates are maximized (e.g., a hump-shaped attack Diversity 2020, 12, 152; doi:10.3390/d12040152 www.mdpi.com/journal/diversity Diversity 2020, 12, 152 2 of 11 rate distribution [17,18]), and the same likely applies to other types of prey traits [19]. Under such a scenario, increasing variance around the optimal trait mean would increase the prevalence of defended individuals, thereby reducing predation rate [11,20]. Alternatively, if the prey population trait mean deviates from the predator’s optimal prey trait value, then increasing variance could increase predation by increasing the prevalence of vulnerable individuals, though this effect would depend on the dominant direction of trait variance [11,20]. These effects of prey trait variance might further depend on predator species identity because predator species often differ in their optimal prey trait values [8,21] as well as the type of selection that they induce (directional, stabilizing, or disruptive) [22]. Trait variance within prey populations could further influence predation rates on other prey species through indirect effects, though the nature of these effects may depend upon the type of phenotypic trait under consideration. If a species’ trait variance directly reduces its vulnerability to predation, then this could turn predation pressure towards other prey species within the community. Alternatively, for traits that are relatively labile, such as behavior, the trait variance of interspecific prey could lead to trait changes in a focal species that render it more vulnerable to predation [23,24]. While this latter indirect effect would not occur with prey traits that are fixed over short durations (e.g., body size), this type of indirect effect could be prevalent for traits whose expression is context-dependent, such as behavior [25]. Nevertheless, the majority of studies examine the effects of prey behavioral traits at the individual level (i.e., a natural selection context) [3], while community-level effects of behavioral trait variance remain poorly understood. Here, we explore how the behavioral trait variances and behavioral trait means of herbivorous insect populations mediate the effects of spider predators on insect survival. We took advantage of naturally occurring boldness (behavioral trait) variation within and across prey populations and manipulated predator species composition to test for context-dependence of behavioral effects. Our study reveals both direct and indirect effects of prey boldness variance, with some effects occurring only under certain spider predator species compositions. These findings demonstrate new pathways by which behavioral trait variation within populations, often overlooked within the field of community ecology [26–28], could scale to regulate community assembly and food web dynamics. 2. Materials and Methods 2.1. Study System and Animal Collection We investigated the effects of prey behavior on prey survival using a spider predator–insect prey community system. Our experiment was conducted in a 60 12 m old-field dominated by × ruderal plants (e.g., Solidago spp.) at the Donald S. Wood Field Laboratory (South Shenango, PA, USA). Spiders are important mesopredators within old-field communities, feeding on a variety of herbivorous insects that in turn regulate old-field primary production [29–31]. Preliminary sampling revealed that the jumping spiders Phidippus clarus and Platycryptus undatus were abundant predators at our field site, while four species dominated the herbivorous insect community: meadow froghoppers Philaenus spumarius, bush katydid nymphs from the genus Scudderia, common meadow katydids Orchelimum vulgare, and silver leafhoppers Athysanus argentarius. Given their abundance and thus high likelihood of interacting in the field, we selected these two predator and four prey species for our experiment. Prior to the experiment, we verified that both jumping spider species fed readily upon these insect prey species in one-on-one feeding trials. Spiders and insects were collected by sweep-netting and maintained individually in 50 mL clear plastic vials before the start of the experiment. Spiders were fed houseflies ad libitum during this 4 day housing period, while insect vials contained a single Solidago canadensis leaf for food and moisture. Individual spiders and insects were used once in the experiment, and survivors were released. Diversity 2020, 12, 152 3 of 11 2.2. Experimental Design We tested the effects of insect prey behavioral trait variances and behavioral trait means on prey survival within replicate field mesocosms. Each 0.36 m2 area mesocosm was stocked with the same insect prey community: 10 Philaenus individuals, 10 Scudderia individuals, 5 Orchelimum individuals, and 5 Athysanus individuals, reflecting the relative abundance of these species at our old-field site. Prior to the placement of insect prey in mesocosms, we assayed the boldness behavior of each individual insect using the same assay (see Prey Behavioral Assay below). Insect prey were then added to mesocosms haphazardly and blindly with respect to their individual behavior (Figure1) in order to generate naturally occurring behavioral variation within and across prey species’ populations. Thus, mesocosm prey communities varied continuously in prey species’ mean boldness and boldness variance. Figure 1. Histograms depicting boldness measurements for insect prey individuals used in the mesocosm experiment. Each mesocosm received 10 Philaenus individuals, 10 Scudderia individuals, 5 Orchelimum individuals, and 5 Athysanus individuals. Prey individuals were added haphazardly and blindly to mesocosms with respect to their individual behavior, generating naturally occurring behavioral variation within and across prey species’ populations. We manipulated spider predator species composition across mesocosms to test whether potential effects of insect prey behavior on prey survival were context dependent (i.e., only occurred under certain predator species compositions). We manipulated spider species composition using three different
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