Monospecific stands of invasive plants can dramatically restructure habitat for fauna, thereby elevating population densities or promoting foraging of consumer species who benefit in the altered habitat. For example, dense stands of invasive plants may protect small mammals from predators, which in turn could increase foraging pressure on seeds that small mammals feed upon. We used a before-after, control-impact experimental design to test whether small mammal capture rates were higher and giving-up densities (GUDs) lower beneath dense stands of Berberis thunbergii, an invasive shrub with a rapidly expanding range throughout eastern North America. Our experimental design included three plot categories: 1) plots heavily invaded by B. thunbergii, 2) control plots lacking invasive shrub cover, and 3) invaded plots where we eradicated B. thunbergii midway through the study. Although our overall small mammal capture rate was low, small mammal captures were 65% higher in B. thunbergii invaded habitat relative to control plots and eradication lowered capture rates by 77%. GUDs were also 26% higher within B. thunbergii relative to control plots and eradication decreased GUDs by 65%. Our findings suggest that small mammals perceive dense stands of B. thunbergii as relatively safe foraging habitat. Prior surveys within our study locations revealed dramatically depressed tree seedling densities under B. thunbergii, thus invasive plants may promote intensive foraging by small mammals and reduce recruitment for species with foraged seeds or seedlings.

Berberis thunbergii, foraging, giving-up density, recalcitrant understory, small mammals

Nonnative plant species that become invasive frequently form dense, nearly monospecific layers that can cause substantial declines in native plant species abundance and diversity. One mechanism that may underlie these declines is that invasive species may commonly provide privileged foraging areas, whereby vertebrate seed and seedling predators gain refuge from their enemies (Orrock et al. 2009; Orrock et al. 2015; Guiden and Orrock 2017). Thus, seed predation by small mammals may be much greater beneath dense layers of invasive plant species than in nearby uninvaded patches. Consequently, any reduction in the diversity and abundance of native plant species could be caused by habitat-mediated predation rather than interspecific resource competition between exotics and natives (e.g., Royo and Carson 2005, 2008; Durra et al. 2011). For example, both experimental (Dutra et al. 2011) and observational (Mattos et al. 2010) studies have demonstrated that dense layers of the invasive Amur honeysuckle (Lonicera maackii) protected small mammals from predators, thereby resulting in elevated foraging event frequencies.

Habitat-mediated predation may be a common phenomenon throughout eastern North American forests because many common invasive plant species are understory shrubs or small trees known to form dense stands (see reviews by Royo and Carson 2006; Richardson and Rejmánek 2011). Common invasive trees or shrubs include several species of honeysuckle (Lonicera spp.), glossy buckthorn (Rhamnus cathartica), Chinese privet (Ligastrum sinense), autumn olive (Eleagnus umbellata), burning bush (Euonymus alatus), and Japanese barberry (Berberis thunbergii) among several others. Elevated seed predation has been well-investigated beneath dense stands of native species, however, whether dense understory layers of invasive shrub species typically create preferred habitats for small mammals remains unclear because there are too few studies to draw any firm conclusions (Orrock et al. 2015). Moreover, non-native species may lead to declines in small mammals if they provide fewer seed resources compared to the native species they displaced. Here, we focus on one of the most widespread and pernicious invaders, Japanese barberry, and evaluate whether barberry creates privileged foraging grounds across three different urban forests using a rigorous BACI experimental design (see below).

Japanese barberry (Berberis thunbergii, hereafter referred to as barberry) is a woody shrub native to East Asia that represents a key model species for investigating cascading effects of invasive, shrubs. Barberry was introduced to North America in the late 19^th century and has spread to at least 32 U.S. states and 6 Canadian provinces (USDA, NRCS 2017). The shrub often forms dense stands that cause both structural and functional shifts in forest understories (Clark and Seewagen 2019). Recalcitrant barberry stands typically reduce temperatures and increase humidity, soil pH, and available soil nitrate relative to uninvaded areas (Kourtev et al. 1999, 2003; Williams and Ward 2010; Link et al. 2019). As with many invasive shrubs (Collier et al. 2002; Flory and Clay 2010), dense barberry patches are often associated with precipitous declines (>33% for certain species) in the abundance of native flora (Kourtev et al. 1998). Silander and Klepeis (1999) attributed declines in native species to interspecific competition for light, however, they did not consider if seed and seedling predators might be partly responsible. At two of our study locations (see below), Link et al. (2018) found a dramatic reduction (82%) in native tree seedling density beneath barberry canopies. They hypothesized that these reductions may have been due to seed predators because tree seedlings transplanted under barberry canopies, thus bypassing the vulnerable seed and small seedling phase, grew at similar rates relative to those planted in nearby controls (Link et al. 2019). Williams et al. (2009) did not detect higher small mammals’ capture rates beneath barberry patches but they focused on only a single target species rather than entire small mammal assemblages. Nonetheless, a few studies suggest that the presence of invasive shrubs (such as Rhamnus cathartica and Lonicera maackii in North America) promotes small mammal foraging activity (Orrock et al. 2015, Guiden and Orrock 2017, Guiden et al. 2019).

Here, we tested the hypothesis that small mammals would be more abundant beneath dense barberry patches or would forage longer in these patches or both. We quantified foraging intensity by estimating giving-up densities (GUDs), defined as the proportion of seeds consumed when mixed with an inorganic substrate (Bedoya-Perez et al. 2013). We predicted that 1) small mammal capture probability would be higher beneath dense patches of barberry, 2) experimental removal of barberry would decrease the capture of small mammals, 3) GUDs would be lower in patches that lacked a dense canopy of barberry or where barberry had been removed, and 4) our results would not vary significantly among three forest reserves separated fairly widely in space. The latter prediction goes to the issue of generality and, if true, suggests that our results are less likely to be location-specific. We used a before/after, control/impact (BACI) experimental design where patches of dense barberry were cleared midway through our field season to assess if removing an invasive regulated the foraging of vertebrate seed predators.

We captured 23 small mammals in total: eight Peromyscus leucopus, ten Peromyscus maniculatus, four Tamias striatus, and a single Blarina brevicauda. Prior to the barberry removal treatment, capture probability significantly varied among the three study locations but not among experimental treatments (Table 1). However, during the period following barberry removal, capture probability was marginally statistically significantly different among treatments, with capture probability elevated in invaded plots relative to control and treatment plots (Table 1, Figure 2A). Before barberry removal, GUDs varied among study locations but not treatments (Table 1, Figure 2B). Following barberry removal, GUDs declined overall and did not vary among locations but values were statistically significantly greater in invaded plots relative to control and barberry removal plots (Figure 2C). No models included statistically significant terms for interactions between treatment and location.

Figure 2.

A Mean capture rates of small mammals during the period after experimental barberry removal delineated by plot type. The horizontal line illustrates the mean capture rate across all locations and treatments during the period prior to experimental barberry removal B mean (± 95% confidence intervals) giving-up densities delineated by location before the experimental barberry removal and C by treatment type for the period after barberry removal. The line and associated gray ribbon illustrate the mean ± 95% confidence interval for giving-up densities across all treatments and locations before barberry removal.

Results affirmed our hypotheses and provide evidence that small mammals forage more aggressively under invasive shrub canopies. During the latter half of the field season, both the small mammal capture probability and GUDs were significantly higher in plots with recalcitrant barberry layers relative to both control plots and plots where barberry was removed. Differences in capture probability and GUDs were not detected in the first half of the field season and we observed a decrease in small mammal GUDs between early and late summer. However, comparable seasonal patterns in activity have been observed for at least P. leucopus in similar ecological settings elsewhere (McMurry et al. 1996). Although we cannot rule out the possibility that the activity of removing barberry itself altered the behavior activity of small mammals after the event, dependent variables in control plots lacking barberry were nearly identical to barberry-removed plots during the second half of the field season. Therefore, we conclude that small mammal foraging activity under barberry canopies is elevated relative to forest floors lacking the invasive species.

Dense patches of a suite of invasive shrub species are now widespread throughout much of the Eastern Deciduous Forest Biome of North American and often cause major declines in native plant diversity (see introduction). Research exploring the mechanisms behind these patterns to date has typically attributed declines in diversity to interspecific resource competition between nonnative shrubs and native species, biological or chemical changes to soil environments that occur after invasion, or invasive species-driven allelopathic effects (Hierro and Calloway 2003; Morales and Traveset 2009; Skurski et al. 2014). Our findings, and those of several others (Mattos and Orrock 2010; Dutra et al. 2011; Malo et al. 2013; Guiden and Orrock 2019) provide an alternative, though not mutually exclusive, explanation. Specifically, seed and seedling predation reduces flora diversity because small mammals occur more frequently and forage longer beneath dense shrub patches, thereby promulgating apparent competition (Holt 2017) between invasive and native flora. The phenomenon is not limited to nonnative taxa: indeed, dense understories of native shrubs and ferns also increase the activity of small mammals and levels of seed predation (Yahner 1986; Carey and Harrington 2001; Castleberry et al. 2002; Spencer et al. 2005; Royo and Carson 2008).

Nonetheless, nonnative shrubs may be more likely to create dense understory layers than native plant species because herbivores typically avoid them (Grosholz 2010; Averill et al. 2016). In our case, barberry may provide particularly effective cover from enemies because it has thorns and it grows via multiple stems that radiate densely from a central root crown (Gleason and Cronquist 1991; Ehrenfeld 1999). Overall, our results, combined with those of others, suggest that the spread of numerous nonnative shrubs across eastern forests, may increase predation pressure on vulnerable seeds and seedling across broad regions wherever these shrubs occur and are abundant. Because of ubiquity of invasive woody plants globally (Royo and Carson 2006; Richardson and Rejmánek 2011), our findings could apply beyond the eastern U.S., and call for replicated experiments in invaded areas worldwide.

Other mechanisms whereby nonnative shrubs increase the abundance or foraging activity of small mammal activity exist beyond providing dense cover. Invasive species may augment small mammal populations if they produce edible fruits and seeds (Orrock et al. 2015). In our case, barberry produces a fruit that is palatable to birds and mammals (Silander and Klepeis 1999; Hayes and Holzmueller 2012) and thus may be augmenting food resources. However, dense patches of invasive shrubs may not always enhance the abundance and foraging activity of small mammals (Hayes and Holzmueller 2012). For example, nonnative shrubs can reduce the abundance of native plant species that are key food resources, or the nonnatives displace native woody vegetation that provided better cover than the nonnative shrubs (e.g., large seeds; Lambrinos 2000; Ostoja et al. 2009; Freeman et al. 2014; Lucero and Callaway 2018). Overall, dense patches of nonnative shrubs can increase small mammal abundance or concentrate foraging because they provide dense cover, the cover extends earlier or later during the growing season, or the nonnatives augment food resources.

Prior investigations in our study locations have detected evidence that seed or seedling predation causes the low densities of native tree seedlings beneath barberry understories. Specifically, Link et al. (2018, 2019) bypassed the seed germination and early establishment phase by transplanting tree seedlings (> 20 cm tall) under barberry and within adjacent control areas lacking barberry. No differences in the survival or growth rates of Quercus spp. and Prunus serotina seedlings between barberry patches and control patches lacking barberry were detected, suggesting that vertebrate seed and seedling predators kill seeds or young seedlings, whereas larger individuals are less vulnerable, though alternative explanations cannot be ruled out (e.g., allelopathy). Still, Guiden and Orrock (2017) and Bartowitz and Orrock (2016) found that an invasive shrub (Rhamnus cathartica) provided cover for small mammals, which increased rates of seed predation rates from 60 to nearly 100%. Furthermore, if the seeds or foliage of dominant invasive species are unpalatable, this may increase rates of seed predation and herbivory on any remaining native plant species growing nearby (Orrock et al. 2008; Dangremond et al. 2010). Regardless, vertebrate seed and seedling predation may be a common mechanism underlying some of the declines in native plant species diversity, particularly woody species with larger seeds (Bartowitz and Orrock 2016).

Seasonal changes in population densities, resource availability, and perceived cover from predation may mitigate how recalcitrant invasive plant cover affects small mammals. Such findings suggest that, during certain seasons, the effects of an invasive plant on foraging activity may diminish. Barberry leaves were present during our entire study period. However, nonnative shrubs may leaf out earlier in the spring and senesce later in the fall than native species, thus extending the phenological window whereby these nonnatives provide small mammals a refuge. Nocturnal light intensity (Prugh and Golden 2014; Guiden and Orrock 2019) and the relative abundance of palatable seeds from canopy trees (Schnurr et al. 2002), neither of which were controlled for in this study, may also significantly impact small mammal foraging behavior. Predation risk may also vary with perceived food quality, as higher-quality resources can result in greater risk-taking (Utz et al. 2016). Therefore, the effects of recalcitrant invasive species cover on small mammals may not be as strong during evenings with low moon luminescence, especially during heavy mast years.

Our findings highlight the potential for elevated foraging intensity in a key faunal assemblage resulting from invasive plants that form recalcitrant understories. Prior studies (Link et al. 2018, 2019) conducted in our field locations revealed depressed tree seedling densities under barberry but transplanted seedlings planted under barberry survived and grew at rates similar to control subjects. Such results, in combination with those presented here, suggest that small mammal foraging may be limiting recruitment of native trees or other heavily foraged plant taxa. Thick understory growth of R. cathartica, another invasive shrub spreading through temperature deciduous forests of North America, also elevates small mammal foraging rates and reduces the abundance of foraged native plants as a result (Guiden and Orrock 2017). However, very few studies have addressed such hypotheses despite the large number of invasive shrubs currently spreading through forest understories in North America and elsewhere.

The authors thank the Falk Foundation for financial support for this effort, Fabiana Licata, Quentin Rice, and Melanie Fetsko for support with field work, and the Allegheny Land Trust and Latodami Nature Centers for generously allowing access to their reserves. Harold Auge, Trinity Smith, and Bruce Osborne provided excellent feedback on earlier drafts of this work.