In a long-term experimental demography study,excluding ungulates reversed invader's explosive population growth rate and restored natives

A major goal in ecology is to understand mechanisms that increase invasion success of exotic species. A recent hypothesis implicates altered species interactions resulting from ungulate herbivore overabundance as a key cause of exotic plant domination. To test this hypothesis, we maintained an experimental demography deer exclusion study for 6 y in a forest where the native ungulate Odocoileus virginianus (white-tailed deer) is overabundant and Alliaria petiolata (garlic mustard) is aggressively invading. Because population growth is multiplicative across time, we introduce metrics that correctly integrate experimental effects across treatment years, the cumulative population growth rate, λ_c, and its geometric mean, λ_per-year, the time-averaged annual population growth rate. We determined λ_c and λ_per-year of the invader and of a common native, Trillium erectum. Our results conclusively demonstrate that deer are required for the success of Alliaria; its projected population trajectory shifted from explosive growth in the presence of deer (λ_per-year = 1.33) to decline toward extinction where deer are excluded (λ_per-year = 0.88). In contrast, Trillium’s λ_per-year was suppressed in the presence of deer relative to deer exclusion (λ_per-year = 1.04 vs. 1.20, respectively). Retrospective sensitivity analyses revealed that the largest negative effect of deer exclusion on Alliaria came from rosette transitions, whereas the largest positive effect on Trillium came from reproductive transitions. Deer exclusion lowered Alliaria density while increasing Trillium density. Our results provide definitive experimental support that interactions with overabundant ungulates enhance demographic success of invaders and depress natives’ success, with broad implications for biodiversity and ecosystem function worldwide.Steadily increasing pressure by invasive plant species on native biodiversity (1) disrupts both community and ecosystem function (2) and results in staggering economic costs worldwide (3, 4). A major goal in ecology is to understand how changes over time in species interactions affect invasion success of exotic species (5–8). According to ecological theory, the ability of the resident community to limit the success of invading exotics biotic resistance (9, 10)] will depend upon ecological context that includes the suite of local interactors (11–15). The abundance of herbivores and their local impacts (11, 14, 16) can play a prominent role in how fast plant populations grow or shrink and how much the relative abundance of plant species changes over time (5, 15), including changes associated with plant invasions (11, 16–19). Recently, increased browsing pressure by overabundant ungulate herbivores on native plant communities has been proposed as a fundamental cause of a shift from native to exotic plant domination in forests and rangelands worldwide (11, 16, 20). Wild and domesticated ungulates (e.g., deer, elk, goats, sheep, horses, cows) that are either native or introduced have all been implicated in this process (11, 16, 20).Overabundant ungulates may change the success of invading exotics in numerous ways. Ungulate browsing on natives may depress their abundance and ability to compete (21–24) and increase abiotic resources available to invaders (11, 25, 26), which can act synergistically to decrease communities’ ability to resist invasion (biotic resistance; refs. 8 and 10). Ungulates disperse exotic seeds (27, 28) and create novel abiotic conditions with respect to soil disturbance, soil quality, and light availability (21, 22, 26), which may enhance exotic establishment and growth. Moreover, although ungulates are considered diet generalists, in fact, they frequently behave as selective foragers (21–24, 29), preferring natives to exotics. In this circumstance, unpalatable invaders can have a double advantage over natives—both release from historic enemies (20) and inedible to new potential enemies in the invaded range (30, 31). Together, these mechanisms not only implicate overabundant ungulates in their direct impact on the rate at which populations of palatable native species grow or shrink, but point to their potentially pivotal role in reducing the biotic resistance of the native community to favor invaders (13, 14).To determine how ungulate herbivores affect the fitness of invaders and natives, field experiments that manipulate herbivore access for several years and are spatially well replicated are required (11, 32, 33). The multiyear, population-level demographic data gained in such experiments can be used to estimate the ultimate metric of fitness: population growth rate (λ). However, despite the widespread use of manipulative experiments that alter herbivore access to plants, we still lack appropriate demographic data (i.e., complete schedules of fertility, mortality and growth for all stages) in invaded systems (2, 14, 17, 32, 33). Instead, herbivore–plant invader experiments typically report simple metrics of plant success (e.g., percent cover or counts of individuals) at a single time point. For example, the metric “percent cover” estimates the total leaf area of a species, often relative to other species. Lower leaf area of native plants where ungulates have access could merely be the result of leaf tissue lost to herbivory, with no actual change in invader or native numbers. Likewise, “snapshot counts” of invaders often leave out critical life cycle stages and do not provide information on rates of survival, reproduction, or growth, without which population dynamics cannot be analyzed. Thus, it is not surprising that ungulate exclusion experiments that apply such metrics provide no unified answer regarding exotic invaders effect on invasion success: none (34–36); mixed (37, 38); positive (39–41; reviewed in ref. 16)] because these studies cannot address population viability of invaders or natives. Also, although evidence of ungulates’ influence on native plant population dynamics from exclusion experiments has been previously demonstrated (e.g., refs. 42 and 43), our study is distinct. We know of no other such experiments testing the link between ungulates and invasive exotic population growth rate in invaded systems.Here, we use experimental demography and stage-based data (rates of survival, fertility, and growth) collected over multiple years to test the hypothesis that an overabundant native ungulate herbivore drives positive population growth of invaders (11, 16). We emphasize that in herbivore removal experiments the fitness of plant populations, which is measured by population growth rate, is predicted to rebound with persistent, multiplicative beneficial effects over time. What has not previously been recognized in such experiments is that treatment effects accumulate over the span of an experiment (44), necessitating a quantitative metric that integrates fitness over the entire life cycle and over time. Moreover, population growth is a process that is multiplicative across time. Thus, we introduce the use of cumulative population growth rate, λ_c, at the end of a multiyear experiment as the metric that correctly integrates experimental effects across the observed sequence of demographic changes across time. Our multiyear demographic projection and the corresponding multiyear retrospective sensitivity analysis provide fresh insights. To facilitate comparisons of our results with studies that estimate λ from single-year transitions, we present λ_per-year, the geometric mean of λ_c. Our retrospective sensitivity analyses similar to life table response experiment analysis for periodic matrices (45, 46)] of λ_c reveal how each part of the life cycle contributes to overall differences in cumulative population dynamics caused by an experimental manipulation. We conclusively show that overabundant deer create conditions favorable for explosive exponential population growth of an exotic plant invader, but that when deer are excluded, populations of the invader are projected to decline exponentially.We focus on the native ungulate Odocoileus virginianus (white-tailed deer; hereafter, deer) and the exotic herbaceous understory invader Alliaria petiolata (Brassicaceae; garlic mustard; hereafter, Alliaria), which both present serious management concerns in North American forests. Relative to historical records, deer densities are currently 4–10 times higher than pre-European settlement densities across North America (47). Overabundant native deer in forests exert the same kinds of pressures as other ungulates (native and nonnative, wild and domesticated) globally, including perturbation of understory communities (22, 27, 39), exotic seed dispersal (27), and alteration of abiotic conditions (21, 39). Likewise, Alliaria ranks among the most problematic forest invaders in North America (48). Introduced by early colonists, it was naturalized on Long Island, New York, by 1868 (reviewed in ref. 48). In its native Eurasia, Alliaria grows in edge or disturbed habitats, whereas in North America it increasingly occupies forest interiors (48). Relative to the slow-growing, long-lived understory community it invades, Alliaria has a rapid, biennial life cycle: spring seedlings form overwintering rosettes by autumn. In their second year, plants reproduce, disperse seeds, and die. In its invaded range, Alliaria has high population growth rates (λ = 1.4–3.4) (48), which project annual increases in numbers of 40–240%. Alliaria’s invasive success has been hypothesized to result from various factors. These include the following: novel allelopathic weapons, enemy release, positive soil feedback, taxonomic novelty, high competitive ability, and specific phenotypic traits. No single factor has yet to explain the broad reach of this tenacious exotic (reviewed in ref. 48). Here, we investigate what has not been previously explored: the role of ungulate disruption of native community biotic resistance (13) on Alliaria’s invasion success. To date, deer and Alliaria have been foci of intense, largely separate, research efforts. Our approach uses experimental demography to jointly examine these two issues. Together, they constitute an ideal system to investigate ungulate–exotic plant invasion linkages (11, 16).Our experiment was conducted in a beech–maple forest in southwestern Pennsylvania (Trillium Trail Nature Reserve, Allegheny County, Pennsylvania: 40° 52′ 01.40″ N; 79° 90″ 10.75″ W). Winter aerial flyovers of this area performed between 1993–2004 revealed overabundant deer: currently 20–42 deer per km² compared with an historic density of 10–12 deer per km² (Fig. S1). In a different area in this same forest, Knight et al. (39) used an indirect metric of plant performance and found that relative percent cover of Alliaria was lower and that there was significantly less bare ground where deer were excluded relative to sites where deer were present (39). However, in that study Alliaria nevertheless remained abundant (the second most abundant species) even where deer were excluded. That study (39), which used relative percent cover as a response metric, left several questions unanswered, including the following: Was Alliaria’s relative decline due to the native species increasing in cover with no actual change in cover of the invader? Did the tenacious invader’s population growth rate actually decline? Given these unanswered questions from the earlier study, the Trillium Trail forest was an ideal location to address these questions and to conduct a definitive demographic experiment that could distinguish among these mechanisms. In 2002, we established paired plots (n = 6 pairs of 14 × 14-m plots) with one plot per pair randomly assigned to a fenced treatment that excluded deer (see Materials and Methods for details). The other plot in each pair remained unfenced and experienced ambient levels of deer and other animals. We compared population-level responses of native understory herbaceous perennial species and Alliaria between treatments for 6 y. For three focal native herbs that are palatable to deer (e.g., ref. 49) and the unpalatable Alliaria, we quantified reproductive success each year. For Alliaria and one of the natives, Trillium erectum (Melanthiaceae, hereafter Trillium), we additionally quantified the complete schedule of survival, fertility, and growth rates each year. We selected Trillium as a counterpoint to Alliaria as it is the most common flowering herbaceous species found at Trillium Trail Nature Reserve. Moreover, Trillium species are a preferred food source for deer (49) and well-known phytoindicators of deer browse (e.g., ref. 49; but see ref. 50). In a nonexperimental study, deer browse levels within a population were negatively correlated with population growth rate for another species in the genus, Trillium grandiflorum (51). Accordingly, Trillium represents a model for understanding the impact of deer on native species, and the loss of such browse-sensitive species can be a metric of decline in forest integrity (52). We predicted that, if ungulates disrupt the native community and enhance exotic invasion success, then in plots experimentally protected from deer: (i) native species would have higher reproductive success, (ii) Trillium fitness would increase and its density would increase, (iii) Alliaria fitness would decrease and its density would decline. Meanwhile, in plots where deer were allowed access, we expected either the opposite trends or no change from initial conditions. Alternatively, if any of the other previously hypothesized mechanisms for Alliaria’s success (e.g., novel weapons, enemy release) are at play and more important than herbivore impacts, then we would expect Alliaria’s population growth rate to remain high despite deer exclusion, while predictions for the effects of deer on the natives remain the same.In brief, from 2003 to 2008 at annual censuses, we scored reproduction and survival of individuals of Alliaria and of the three native perennials that are preferred food sources for deer (49): Trillium, Maianthemum racemosum (Ruscaceae), and Polygonatum biflorum (Ruscaceae). In plots accessible to deer, we also scored deer browse. To assess the effect of deer exclusion on the fitness of Trillium and Alliaria, we implemented our multiyear matrix projection analysis to calculate cumulative population growth rates from 2003 to 2007 for each treatment. To construct matrices, we defined five life cycle stages for the perennial Trillium (germinant bank, seedling, one-leafed juvenile, three-leafed nonflowering, and three-leafed flowering; Fig. S2A) and three life cycle stages for Alliaria (dormant seed in the seed bank, rosette, and fruiting adult; Fig. S3A). Matrix elements were calculated as a function of the vital rates associated with each stage transition (Figs. S2A and S3A). We captured cumulative effects of deer exclusion or continued deer overabundance over time, parameterizing multiyear projection matrix models B, for each species and treatment by multiplication of annual projection matrices A_{YEAR-TREATMENT} (e.g., B_DEER = A_2006-DEER A_2005-DEER A_2004-DEER A_2003-DEER). The matrix B, at the heart our analyses, contains the rates at which individuals that were at a given stage at the beginning of the experiment will have either become or produced individuals of each stage after four transition years. Our analyses of multiyear matrices provide integrative measures of plant fitness over the time frame of the experiment, including treatment-specific cumulative population growth rates (λ_c, the dominant eigenvalue of B), time-averaged λ’s (λ_{per-year-TREATMENT} = the fourth root of the dominant eigenvalue, λ_c, of B), and an overall measure of the effect of protecting plants from deer on plant fitness Δλ_per-year = λ_{per-year-NO_DEER} – λ_{per-year-DEER}. Note: Pooled plot data (Trillium) and individual plot data (Alliaria) were used. See Materials and Methods, Matrix Construction for Each Species and Treatment.] Finally, to uncover mechanistic differences between the response of the native and the exotic to deer exclusion, we use a life table response experiment retrospective sensitivity analysis (45, 46). The analysis shows how important each of these 4-y demographic rates is to differences in λ_c between treatments, quantified by contributions made during transitions from stage j to stage i, c_ij.