White-Tailed Deer Alter Specialist and Generalist Insect Herbivory Through Plant Traits

Abstract

Within a plant species, leaf traits can vary across environmental, genetic, spatial, and temporal gradients, even showing drastic differences within individuals. Herbivory can also induce variation in leaf morphology, defensive structure, and chemistry including nutritional content. Indirect effects of prior insect herbivory on later herbivores have been well documented, but the induction of trait changes after vertebrate herbivory has been little explored. Here, we examined how browsing of spicebush (Lindera benzoin L.), a dominant understory shrub in eastern mesic forests, by white-tailed deer (Odocoileus virginianus L.) altered plant quality and subsequent foliar herbivory by insects. Browsing history explained ≈ 10% of overall leaf trait variation; regenerated leaves had greater water content and specific leaf area (P = 0.009), but were lower in nitrogen and greater in carbon (P < 0.001), than leaves on unbrowsed plants. However, browsing did not shift terpene chemistry as revealed by GC-MS. In the lab, caterpillars of the specialist spicebush swallowtail (Papilio troilus L.) preferred (P = 0.02) and grew 20% faster (P = 0.02) on foliage from browsed plants; whereas total herbivory in the field, including generalist insect herbivory, was twice as high on unbrowsed plants (P = 0.016). These results suggest that the ecological impacts of deer in forest understories can have cascading impacts on arthropod communities by changing the suitability of host-plants to insect herbivores.

Long-term deer exclosure alters soil properties, plant traits, understory plant community and insect herbivory, but not the functional relationships among them

“…Deer browsing can reduce plant traits, such as plant height, number of shoots (Den Herder et al 2004), number of leaves per plant (Takagi and Miyashita 2012), and leaf N content (Lind et al 2012). Nonetheless, occasionally deer browsing may actually increase foliar nutrient content (Takagi and Miyashita 2012).…”

“…Takatsuki and Itô (2009) showed that high densities of deer inhibited tree regeneration and favored understory plant communities composed of highly herbivory-tolerant and well-defended species. Furthermore, changes to plant properties induced by deer presence can have positive (Barrett and Stiling 2007; Takagi and Miyashita 2012) or negative (Lind et al 2012; Shimazaki and Miyashita 2002) effects on the attack of these plants by other herbivores. The direction of these indirect plant-mediated interactions induced by deer can be similar or different across different insect-feeding guilds (Poelman et al 2010; Viswanathan et al 2005).…”

“…This is because the absence of deer herbivory typically leads to increased foliar nutrient concentrations (Lind et al 2012), lower leaf toughness (Coley 1983; Lambers and Poorter 1992) and decreased plant defense (Shikata et al 2013), which is favorable to insect herbivores (Lind et al 2012; Takagi and Miyashita 2015); (2) more S. palmata individuals per area as the result of deer absence (Nishizawa et al 2016) will dilute the increase in insect herbivory, leading to lower insect herbivory per plant; (3) damage by different insect-feeding guilds to S. palmata will be affected differently by sika deer grazing due to disparate resource requirements between guilds (i.e., specialist versus generalist herbivores) (Barrett and Stiling 2007); (4) the functional relationships between soil properties, the plant community and the traits of S. palmata will be altered due to deer exclosure, thereby impacting on insect herbivory. This is because deer presence is known to alter plant traits (Karban 2011; Ohgushi 2005), soil properties (Abbas et al 2012; Kardol et al 2014) and the understory plant community (Nishizawa et al 2016; Takatsuki and Itô 2009; Wardle et al 2001) in ways that can drive insect herbivory via indirect trophic interactions (Fig.…”

Spatially distinct responses within willow to bark stripping by deer: effects on insect herbivory

“…Thus, herbivory by one herbivore can alter the food quality of plants for other herbivores, positively or negatively affecting their performance, density, and/or patterns of herbivory (Gange and Brown 1989;Roininen et al 1997;Martinsen et al 1998;Nakamura et al 2003;Lind et al 2012). Many studies on these Bplant-mediated effects^have investigated plant parts (e.g., leaves and shoots) close to the site of herbivory (Danell and Huss-Danell 1985;Roininen et al 1997;Martinsen et al 1998;Nakamura et al 2003;Bailey and Whitham 2006;Lind et al 2012), on the assumption that induced responses tend to be stronger closer to the damage. In contrast, several authors have reported that herbivory by one herbivore can positively or negatively affect other herbivores that are distant from the damaged site due to changes in resource allocation at the whole-plant scale (Gange and Brown 1989;Bezemer et al 2003;Johnson et al 2013).…”

“…The overabundance of sika deer results in heavy herbivory pressure (e.g., browsing, bark stripping, grazing) on vegetation, especially on preferred plants such as willows (Salix udensis and Salix miyabeana). There is increasing evidence that cervid herbivory induces compensatory regrowth in plant parts close to those damaged by herbivory (Danell and Huss-Danell 1985;Roininen et al 1997;Bailey and Whitham 2006;Lind et al 2012). The regrowth response following cervid herbivory often facilitates insect herbivory (Danell and Huss-Danell 1985;Roininen et al 1997) because it provides new plant tissues, which tend to contain greater nitrogen and are often poorly defended (Danell and Huss-Danell 1985;Nakamura et al 2006).…”