Mammalian Herbivores As Drivers of Community Assembly

Home , Assembly rules, Limiting similarity

Mammalian Herbivores as

Drivers of Community Assembly

Caprice M. Disbrow

A thesis submitted to

Sonoma State University

in partial fulfillment of the requirements

for the degree of

MASTER OF SCIENCE

Biology

Committee members:

Dr. Daniel E. Crocker, Chair

Dr. Lisa Bentley

Dr. J. Hall Cushman

Dr. Marko J. Spasojevic

April 20, 2018

By Caprice M. Disbrow

Authorization for Reproduction of Master’s Thesis

Permission to reproduce parts of this thesis must be obtained from me.

DATE: April 20, 2018 NAME: Caprice M. Disbrow

iii

Mammalian Herbivores as Drivers of Community Assembly

Thesis by Caprice M. Disbrow

ABSTRACT

Despite growing interest in trait-based approaches to community assembly, little attention has been given to mammalian herbivores and their effects on trait distribution patterns. Large herbivores can play a key role in structuring communities, affecting community assembly though their role as consumers, depositors of metabolic wastes and as agents of disturbance. This study analyzes the effect of a native, reintroduced herbivore on taxonomic and functional trait distributions using a 20-year-old exclosure experiment, stratified across a heterogeneous coastal ecosystem. I found that herbivores can alter the taxonomic diversity, functional composition (CWMs) and functional diversity (FDis) of plant communities, and that their influence may be mediated by the local environmental conditions (soil formation). Importantly, we found significant changes in functional diversity due to elk shifting the dominance of plant species across the landscape even though elk had no influence on species richness. Specifically, I found that elk altered the functional diversity of these plant communities by shifting functional strategies from a stress avoidant strategy to a more resource acquisitive strategy and by deterministically changing functional diversity patterns. Assessing the degree to which herbivores drive community assembly and functional traits has important implications: it provides insights into the mechanisms driving changes in plant communities and has the potential to allow perturbations in communities to be detected and mitigated.

Keywords: functional traits, plant community ecology, native ungulate herbivores, environmental heterogeneity and community assembly.

MS Program: Biology Sonoma State University Date: April 20, 2018

Acknowledgements

I am indebted to the following individuals for assistance in the lab and field: Cody Ender,

Eric Cecil, Melissa Crews, Vanessa Dodge, Emily Fredrickson, Brieanne Forbes, Megan

Gaitan, Andrew Griffin, Caitlin Harvey, Elias Lopez, Shannon McEntee, Danielle

Wegner and Keith Wellstone. Thanks to Tim Bernot at Point Reyes National Seashore for his help in maintaining the exclosures. David Press and Brent Johnson provided invaluable logistical support throughout the entire project. Special thanks go to Dan

Crocker for his guidance with our statistical analyses and to Lisa Bentley for helpful discussions and comments on early drafts of this thesis. This project has been generously supported by grants from the California Native Plant Society Milo Baker Chapter,

Northern California Botanists and Sonoma State University.

Table of Contents Table of Contents

Introduction ...... 1

Methods ...... 4

Study System ...... 4

Experimental Design ...... 6

Vegetation Sampling ...... 7

Trait Selection and Measurement ...... 7

Diversity Indices ...... 9

Statistical Analyses ...... 10

Results ...... 11

Taxonomic Diversity ...... 11

Community Weighted Mean ...... 11

Functional Diversity...... 12

Discussion ...... 14

Changes in Taxonomic Diversity ...... 14

Changes in Community-weighted Traits ...... 16

Changes in Functional Diversity ...... 18

Effects on Native and Exotic Species ...... 19

Simultaneous Processes and Inferred Mechanisms ...... 20

Conclusions ...... 20

Literature Cited ...... 22

List of Tables

Table 1. Results from ANOVA models evaluating the effects of tule elk and soil formation (SF) on (a) plant species diversity, (b) plant species evenness, (c) plant species richness, (d) percent cover of native species, and (e) percent cover of exotic species. Bold text indicates significant results and italicized text indicates marginally significant results...... 32

Table 2. Results from ANOVA models evaluating the effects of tule elk and soil formation (SF) on (a) CWM SSD (log transformed), (b) CWM height (log transformed). (c) CWM SLA (log transformed), (d) CWM LA (log transformed), and (e) CWM LDMC (log transformed). Bold text indicates significant results and italicized text indicates marginally significant results...... 33

Table 3. Results from ANOVA models evaluating the effects of tule elk and soil formation (SF) on (a) FDis height, (b) FDis leaf dry matter content (LDMC) (log transformed (c) functional dispersion (FDis) stem- specific density (SSD) (log transformed), (d) FDis leaf area (LA) (log transformed), (e) FDis specific leaf area (SLA), and (f) multivariate FDis. Bold text indicates significant results and italicized text indicates marginally significant results...... 34

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List of Figures

Figure 1. Mean (+/- 1 S.E.) plant species diversity H’(a) , plant species evenness (b) and plant species richness (c) as a function of elk (present or excluded) and soil formation (ordered by soil texture from finest to coarsest: Kehoe variant 1, Kehoe variant 2, mixed Kehoe variant 1/Sirdrak Sand, and Sirdrak Sand)...... 36

Figure 2. Mean (+/- 1 S.E.) percent cover of native (a) and exotic (b) plant species as a function of elk and soil formation (ordered by soil texture from finest to coarsest: Kehoe variant 1, Kehoe variant 2, mixed Kehoe variant 1/Sirdrak Sand, and Sirdrak Sand)...... 37

Figure 3. Mean (+/- 1 S.E.) community weighted mean (CWM) of stem- specific density (SSD) (a), community weighted mean of specific leaf area (SLA) (b), community weighted mean of height (c), community weighted mean of leaf area (LA) (d) and community weighted mean of leaf dry matter content (LDMC) (e) as a function of elk and soil formation (ordered by soil texture from finest to coarsest: Kehoe variant 1, Kehoe variant 2, mixed Kehoe variant 1/Sirdrak Sand, and Sirdrak Sand)...... 38

Figure 4. Mean (+/- 1 S.E.) functional dispersion (FDis) of height (a), functional dispersion of leaf dry matter content (LDMC) (b), functional dispersion of stem-specific density (SSD) (c), functional dispersion of leaf area (LA) (d), functional dispersion of specific leaf area (SLA) (e) and multivariate functional dispersion (f) as a function of elk and soil formation (ordered by soil texture from finest to coarsest: Kehoe variant 1, Kehoe variant 2, mixed Kehoe variant 1/Sirdrak Sand, and Sirdrak Sand). Letters above bars correspond to the results from Tukey multiple comparison tests...... 39

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Introduction

Understanding the factors that structure communities is a long-standing goal in ecology, with important implications for restoration and conservation. Large herbivores can play a key role in structuring communities, affecting both plant invasions (Maron &

Vila 2001; Parker, Burkepile & Hay 2006; Gross et al. 2013; Pekin et al. 2015) and community assembly (Crawley 1983; Huntly 1991; Olff & Ritchie 1998; Ohashi &

Hoshino 2014). Despite the demonstrated influence of large herbivores, a growing number of studies have revealed that the magnitude and direction of these effects can be quite variable. For example, large native herbivores are reported to either increase

(McNaughton 1979; Milchunas, Sala & Lauenroth 1987; Huntly 1991; Belsky 1992;

Stewart et al. 2009) or decrease (Hegland, Lilleeng & Moe 2013; Speed, Austrheim &

Mysterud 2013; Lezama et al. 2014) plant species richness, while some studies report little or no effects (Jefferies, Klein & Shaver 1994; Stohlgren, Schell & Heuvel 1999;

Adler et al. 2005; Relva, Nuñez & Simberloff 2010). Similarly, herbivores can also have major effects on plant invasions, although here again, there is a great deal of variability in their effects. Studies have shown that herbivores can both reduce and increase the success of exotic plant invaders (Parker et al. 2006; Johnson & Cushman 2007; Skaer, Graydon

& Cushman 2013; Kalisz, Spigler & Horvitz 2014; Pekin et al. 2015; Ender, Christian &

Cushman 2017a). While documenting these variable responses to herbivores is valuable, understanding what drives the variation is critical for being able to generalize about the effects of herbivores on plant invasions and community composition.

Although most studies evaluating the effects of herbivores on plant communities have employed a taxonomic approach, of which species richness and diversity are the most widely studied components (Milchunas et al. 1987; Olff & Ritchie 1998),

2 expanding the focus to include functional diversity may provide greater or complementary understanding of the mechanisms causing variability in the effects of herbivores on invasion and community assembly (Díaz, Noy-meir & Cabido 2001;

Ricotta & Moretti 2011; HilleRisLambers et al. 2012). For example, species richness may not change in response to herbivores, but the diversity or distribution of functional traits and associated strategies in a community may change (Peco et al. 2012).

Importantly, plant functional traits can be linked to the direct and indirect effects of herbivores on different factors in the community. For example, an increase in the diversity of specific leaf area (the ratio of leaf area to dry mass) among coexisting species is associated with an increase in niche differentiation in response to competition for light and/or soil nutrients (Kraft, Valencia & Ackerly 2008; Dwyer, Hobbs & Mayfield 2014).

If a similar pattern is seen in response to herbivores, this may suggest that herbivores are altering competitive interactions among coexisting species. While there has been a tremendous increase in studies that emphasize functional diversity, relatively few of them have focused on the effects of herbivores. Most have applied a trait-based approach to generalize about vegetation responses (Landsberg, Lavorel & Stol 1999; McIntyre &

Lavorel 2001; Cingolani et al. 2007; Evju et al. 2009; Peco et al. 2012), reporting that herbivores shifted the community so that it was dominated by annual over perennial plants, short plants over tall plants, prostrate over erect plants, and stoloniferous and rosette architecture over tussock architecture (Diaz et al. 2007; Laliberte et al. 2012). Still fewer focus on trait-based examination of native and exotic traits in response to herbivores (but see Gross et al. 2013), and analyses often only consider multivariate functional diversity patterns (Cleland et al.2011, Dainese & Bragazza 2012, Tecco et al.

2010). Other studies have found that these responses can be modulated by a number of

3 factors such as water (Carmona et al. 2012) and nutrient availability (Pastor & Cohen

1997; Laliberte et al. 2012; Niu et al. 2015).

Trait patterns can be influenced by mammalian herbivores in numerous ways, through their activities as consumers, fertilizers, and disturbance agents. If large herbivores influence plant communities primarily through their effects as consumers, functional diversity of plant traits may be reduced by these activities because grazing often selects for an avoidance or tolerance strategy (Chesson 2000; Grime 2006). If herbivores influence plant communities primarily through the deposition of metabolic wastes (fertilizers), these activities will likely increase the functional diversity of plant traits associated with nutrient acquisition, given that increased nutrient availability may increase competition among coexisting species (Diaz et al. 2007). If herbivores influence plant communities primarily through their activities as disturbance agents, this may reduce functional diversity of traits associated with tolerating disturbances, such as stem density or leaf dry matter content. At the same time, small frequent soil disturbances by large herbivores may enhance germination opportunities for plants, thus altering competitive interactions and possibly selecting for increased functional diversity of traits associated with competition for light or nutrients.

A further challenge is that large mammalian herbivores regularly inhabit extensive geographic landscapes that exhibit tremendous spatial variation in a wide range of factors including soil type, nutrient and water availability, productivity, plant community type and composition (Olff, Ritchie & Prins 2002). Environmental heterogeneity in the landscape may be an important factor driving much of the variation in the effects of herbivores on plant invasion and community composition (McNaughton

1983; Gough & Grace 1998; Augustine & McNaughton 2006; Bakker et al. 2006;

Hillebrand et al. 2007). These spatially variable attributes have the potential to mediate the effect of herbivores on plant communities (Adler, Raff & Lauenroth 2001; Young et al. 2013).

Here, I use an 18-year-old exclosure experiment, stratified across a heterogeneous coastal ecosystem, to evaluate the impact of a native, reintroduced herbivore on plant community assembly. Our research addresses the following questions:

1) Do herbivores shift functional dispersion, community weighted means and/or taxonomic diversity indices of plant communities and do these effects vary across soil formations? 2) Do herbivores create nonrandom plant assemblages? Answers to these questions will enhance our understanding of the ways in which herbivores influence the functional and taxonomic diversity of plant communities and provide a mechanistic framework to explain variability in the effects of large herbivores on community assembly.

Methods

Study System

Our research was conducted at Tomales Point, a federally designated wilderness area within Point Reyes National Seashore in Marin County, approximately 65 km northwest of San Francisco. Bordered by the Pacific Ocean and Tomales Bay, Tomales

Point is a 1,030-ha peninsula that experiences a Mediterranean-type climate, with moderate rainy winters and cool, foggy summers receiving very little precipitation. The vegetation of Tomales Point is a mosaic of shrub-dominated coastal scrub and grassland, interrupted by steep canyons containing dense riparian shrubs (Lathrop & Gogan 1985).

The grassland component of Tomales Point consists of both native and introduced

5 herbaceous plant species interspersed with native shrubs. Three distinct soil types as defined by Kashiwagi (1985) as well as a fourth mixed soil type occur within our 300-ha study area: 1) Kehoe variant 138, a coarse sandy loam (derived from Cretaceous granitic parent rock; Wagner et al. 1982, Stoffer 2005) characterized by herbaceous patches mixed with dense stands of Baccharis pilularis (Asteraceae), a long-lived native shrub

(Johnson & Cushman 2007); 2) Kehoe variant 139, a course sandy loam (derived from

Cretaceous granitic parent rock; (Wagner et al. 1982, Stoffer 2005) dominated by herbaceous species and largely devoid of shrubs (Johnson & Cushman 2007); and 3)

Sirdrak sand (derived from a Quaternary dune sand parent rock; Wagner et al. 1982,

Stoffer 2005), dominated by a short-lived, native, nitrogen-fixing shrub, Lupinus arboreus (Fabaceae). The Sirdrak sand and mixed Sirdrak/Kehoe soils are extremely well-drained, resulting in much drier conditions than seen in either Kehoe soil formation

(Dodge, Eviner and Cushman, unpublished data). Two of our experimental plot-pairs are situated on a mixed soil that occurs on the border between Kehoe 138 formation and the

Sirdrak sand. This soil (hereafter referred to as the mixed soil) has properties of both the distinct soil formations as described above as well as areas where the two soils are a heterogeneous mix, depending on where the soil is sampled within the experimental plots.

Tule elk (Cervus canadensis nannodes) is a native ungulate that once dominated much of coastal and central California. These herbivores once numbered 500,000 individuals, but hunting and land conversion during the Gold Rush brought them to the brink of extinction by the mid-1800s (McCullough 1969). The dramatic decline prompted efforts to protect elk, bolster their numbers and reintroduce populations to over 20 different sites in California. In 1978, 10 tule elk were reintroduced to a designated

6 wilderness area on Tomales Point. Following their reintroduction, the tule elk population grew rapidly for two decades, reaching approximately 450 individuals before leveling off. Since 1998, the herd has fluctuated between 400 and 600 individuals, although the

2014 census indicated that the population had declined to fewer than 300 animals, possibly due to prolonged drought (D. Press, unpublished data). The diet of tule elk at

Tomales Point consists primarily of herbaceous forbs and grasses, but they also consume shrub foliage during the winter months when less herbaceous material is available

(Gogan & Barrett 1995). Being large animals (200-250 kg), elk can also create substantial amounts of disturbance to the vegetation and soil.

Experimental Design

This study centers around a large-scale elk exclosure experiment located on

Tomales Point in Point Reyes National Seashore (see illustration below). Established by the National Park Service and U.S. Geological Survey in 1998, the experiment occurs within a 300-ha area and consists of 24 36 × 36 m plots distributed across a habitat gradient and among soil formations as described above. Each plot in the experiment is located 350-850 m from the Pacific Ocean. The 24 experimental plots are organized into

12 pairs, with one plot within each pair randomly assigned fencing to exclude elk and another plot spaced 3 m away left unfenced to serve as a control. Four of these plot-pairs are on Kehoe variant 138, four pairs are on Kehoe variant 139, two are on Sirdrak sand, and two are on mixed Kehoe/Sirdrak soil. The fencing that surrounds each exclosure plot is 2.5-m tall and effectively excludes elk but not other small- or mid-sized herbivores such as deer or hares (J. H. Cushman, personal observation). Other studies using this exclosure experiment have shown that elk exert major influences on the plant community

(Johnson & Cushman 2007), small mammals (Ellis and Cushman, in review), ground- dwelling arthropods (Cecil, Spasojevic, and Cushman, unpublished data), and invasive exotic grasses (Ender, Christian & Cushman 2017b).

Vegetation Sampling

Between May 15th and June 20th of 2016, we quantified plant species composition within the exclosure experiment using a stratified approach. We quantified species-specific plant cover within 12 50 x 50 cm quadrats in each of the 24 plots using the point-intercept method. Quadrats were placed 1 m to the right of, and above, a grid of nine points. At each of 36 points per quadrat, we recorded total number of plant species encountered. In addition, we determined the identity of all plant species occurring in each plot to obtain whole-plot species richness. We restricted vegetation sampling to the central 30 x 30 m area of each plot so as to reduce possible edge effects caused by fencing.

Trait Selection and Measurement

We selected functional traits that are known to be associated with herbivory, resource acquisition and tolerance to environmental stress (Ehleringer & Marshall 1995;

Westoby 1998; Díaz et al. 2001); height, specific leaf area (SLA), leaf area (LA), leaf dry matter content (LDMC), and stem-specific density (SSD). Perez-Harguindeguy et al.

(2013) have compiled theory and justification for correlations between plant traits and physiology, thus this section references their publication. SLA is often positively correlated with relative growth rate across species. SLA also typically scales positively with mass-based light-saturated photosynthetic rate and with leaf nitrogen concentration,

8 and negatively with leaf longevity and carbon investment in quantitatively important secondary compounds such as tannins and lignin. LA is defined as the one-sided area of an individual leaf, expressed as mm2. Interspecific variation in LA has been variously related to climatic variation, geology, altitude and latitude, where heat stress, cold stress, drought stress, nutrient stress and high-radiation stress all tend to select for relatively small leaves. LDMC has been shown to scale positively with leaf lifespan, and leaves with high values tend to be relatively tough, and are assumed to be more resistant to physical hazards (e.g. herbivory, wind, antler thrashing). SSD is emerging as a core functional trait because of its importance for the stability, defense, architecture, hydraulics, carbon gain and growth potential of plants. Stem density partly underlies the growth-survival trade-off – a low stem density (with large vessels) leads to a fast growth because of cheap volumetric construction costs and a large hydraulic capacity, whereas a high stem density (with small vessels) leads to a high survival because of biomechanical and hydraulic safety, resistance against pathogens, herbivores or physical damage

(Santiago et al. 2004, Pérez-Harguindeguy et al. 2013).

In May and June of 2016, we quantified these five traits within each plot in the exclosure experiment. We focused on plant species that collectively contributed to at least 80% of the cover in each plot of the exclosure experiment. For all five traits, we collected data following the methods outlined by Perez-Harguindeguy et al. (2013), the widely recognized authority on this subject. For each focal plant species, we collected five fully formed adult leaves with no signs of damage or senescence at peak biomass.

Collected leaves were stored in floral tubes in sealed plastic bags and were weighed and scanned (to determine area) within 24 hours of collection. Leaf areas were calculated from scans using Image-J (Rasband 2007). Leaves were then dried at 55 C for four days

9 and weighed to determine leaf dry mass. SLA was calculated as leaf area (cm2) per unit of dry leaf mass (g). Additionally, we collected a 10-cm-long section near the base of a branchless stem and wrapped each cutting in moist tissue in plastic bags and stored them in a cool box until measurement. We used the water-displacement method (Pérez-

Harguindeguy et al. 2013) to obtain volume. Stem-specific density is measured as the oven-dry mass of a section of a stem of a plant divided by the volume of the same section when still fresh.

Diversity Indices

To assess the effects of elk on the composition of plant community, we calculated species richness, evenness and Shannon–Wiener (Shannon & Weaver 1949) diversity index (H’) for each plot. We used H’ because it is weighted for abundance and is less correlated with species richness than Simpson’s diversity index. To describe functional composition of the plant assemblage in each plot, we calculated the community-weighted means (CWM), which are plot-level traits weighted by abundances or cover. We calculated functional diversity as functional dispersion (FDis) (Laliberté & Legendre

2010). In multidimensional trait space, FDis is the mean distance of each species, weighted by relative abundances or cover, to the centroid of all species in the community.

While there are currently many metrics of functional diversity available (reviewed by

Mouchet et al. 2010, Schleuter et al. 2010), FDis was the most appropriate for our study because it is independent of species richness, takes into account species abundances/cover, and can be used for single or multiple traits (Laliberté & Legendre

2010). Functional diversity was calculated using the dbFD function in the FD package

(Laliberté & Shipley 2011) in R (R core team 2017).

Statistical Analyses

We analyzed each of the taxonomic plant community response variables

(richness, evenness, and diversity) and each functional index (FDis and CWM) using linear mixed models in JMP 13 Pro (SAS Institute, Cary, NC, USA), with elk (present or excluded), and soil formation (Kehoe variant 1, Kehoe variant 2, Sirdrak sand, and mixed) and their interaction as fixed effects, and plot pair (1-12) nested within soil formation as a random effect. To ensure that assumptions for linear mixed models were met, we visually assessed all model residuals for approximate normality and checked for homoscedasticity of residual plots. If soil formation or any of the interaction terms were significant, we followed up with least square Tukey multiple comparison tests to evaluate differences among the means.

In addition to assessing the influence of elk on functional trait variables using categorical predictor variables (herbivores, soil formation), we also tested for the existence of nonrandom assembly processes due to the effect of herbivores. To accomplish this, we used R (R Development Core Team 2017) to compare observed trait distributions with null model expectations and test for significant community structure that may reflect assembly processes (Cornwell & Ackerly 2009). We used the FD package (Laliberté & Legendre 2010) to calculate CWM and FDis, and the vegan package (Oksanen et al. 2010) to create null communities. We calculated null FDis for each plot and calculated 95% confidence intervals based on 9999 iterations of the null model. Using these, we looked for differences between the observed FDis and null FDis, where positive values indicated greater functional diversity than the null expectation and negative values indicated lower functional diversity than null. These analyses are

11 calculated under the null assumption that the local communities should reflect a random distribution of individuals and traits across a landscape drawn from the regional species pool, weighted by the abundance of the species present at the regional scale.

Results

Taxonomic Diversity

A total of 97 plant species were found in the 24 plots of our exclosure experiment.

Elk increased both plant species diversity (H’) (Table 1a, Figure 1a) and species evenness

(Table 1b, Figure 1b). Neither soil formation nor the elk x soil formation interaction significantly influenced species diversity (Table 1a, Figure 1a) or evenness (Table 1b,

Figure 1b, respectively). Similarly, neither elk, soil formation, nor the elk x soil formation interaction significantly influenced species richness (Table 1c, Figure 1c).

Neither elk nor the elk x soil formation interaction had an influence on native species percent cover in communities (Table 1d, Figure 2a), whereas soil formation did have a significant influence native species percent cover in communities (Table 1d,

Figure 2a). Similarly, neither elk nor the elk x soil formation interaction significantly influenced exotic species percent cover (Table 1e, Figure 2b), although soil formation did show a trend toward influencing exotic species percent cover (Table 1e, Figure 2b).

Community Weighted Mean

Elk significantly decreased the community weighted mean (CWM) of stem- specific density (Table 2a, Figure 3a). The effect of elk did not differ among soil formations (Table 2a, Figure 3a) and soil formation did not have an influence (Table 2a,

Figure 3a). In contrast, elk significantly increased CWM for height and soil formation

12 also influenced CWM for height (Table 2b, Figure 3b). We also found a trend for an interaction between elk and soil formation on the CWM of height (Table 2b, Figure 3b).

Elk had a marginally significant effect on CWM of specific leaf area (Table 2c, Figure

3c), but soil formation did not influence CWM SLA (Table 2c, Figure 3c), and there was no interaction between elk and soil formation (Table 2c, Figure 3c). Neither elk, nor soil formation significantly influenced leaf area and there was no interaction between the elk and soil formation (Table 2d, Figure 3d). Elk significantly increased the CWM of leaf dry matter content (Table2e, Figure 3e); however, CWM LDMC was not influenced by soil formation and there was no interaction between elk and soil formation (Table 2e, Figure

3e).

Functional Diversity

Elk had variable effects on the functional trait diversity of the plant communities I examined. In some cases, communities influenced by elk were less functionally diverse than expected from the null expectation (underdispersed), some did not significantly differ from null expectations, and some had significantly greater functional diversity than expected (overdispersed). Elk generally decreased functional diversity for height (Table

3a, Figure 4a), but this effect depended on soil formation (Table 3a, Figure 4a), where elk had a considerable effect in Sirdrak and mixed soils, a weak effect on Kehoe 2 and no effect on Kehoe 1. Additionally, functional diversity of height varied among soil formations (Table 3a, Figure 4a). Elk caused the functional diversity of height to be overdispersed in two communities with well drained soils (Sirdrak sand and mixed soil formations) in Lupinus-dominated grasslands and to be underdispersed in two communities on Kehoe 2 soil formation in open grasslands.

Elk generally decreased FDis of leaf dry matter content (Table 3b, Figure 4b), that this effect was consistent among soil formations (F3,8=1.66, P = 0.0.2521, Figure 4b) and that soil formation only marginally influenced FDis of LDMC (Table 3b, Figure 4b).

Functional diversity of LDMC was generally not different that the null expectation, with

Elk causing underdispersion of LDMC in only one community on Kehoe 1 soils.

Elk also generally decreased stem-specific density (Table 3c, Figure 4c) that this effect was consistent among soil formations (Table 3c, Figure 4c), and that soil formation did not influenced FDis of stem-specific density (Table 3c, Figure 4c). Functional diversity of SSD was generally not different that the null expectation, with elk causing overrdispersion of SSD in only one community on mixed soils.

I found that functional diversity of leaf area was not influenced by elk, soil formation or their interaction (Table 3d, Figure 4d). However, I still found that leaf area was underdispersed in two communities, one on Kehoe 1 soils and one Kehoe 2 soils, and overdispersed in one community found on Kehoe 1 soils. Similarly, Functional diversity of SLA was not influenced by elk, soil formation, nor their interaction (Table 3e, Figure

4e) and SLA patters did not differ from the null expectation in response to elk or soil formation.

Lastly, I found that elk increase multivariate FDis (Table 3f, Figure 4f), that this effect was largely consistent across soil types (Table 3f, Figure 4f), and did not differ among soil formations (Table 3f, Figure 4f). Multivariate functional diversity was underdispersed in one community where elk were not present and found on Kehoe 2 soil formation.

Discussion

Patterns of functional trait diversity are increasingly being used to detect the signatures of different community assembly mechanisms (Cornwell & Ackerly 2009;

Mouchet et al. 2010; Mason et al. 2011). While these approaches have provided many insights in to the assembly of ecological communities, these approaches have largely focused on horizontal comminutes (same trophic level) and few studies have attempted to integrate the role of herbivores into trait-based community assembly (Adler et al. 2004;

Spasojevic et al. 2010; Peco et al. 2012; Begley-Miller et al. 2014). Here, I found that herbivores can have an effect on the functional composition (CWMs) and functional diversity (FDis) of plant communities, and that their influence may be mediated by the local environmental conditions (soil formation). Importantly, we found significant changes in functional diversity due to elk shifting the dominance of plant species across the landscape even though elk had no influence on species richness. Specifically, I found that elk altered the functional diversity of these plant communities by shifting functional strategies from a stress avoidant strategy to a more resource acquisitive strategy and by deterministically changing functional diversity patterns. Together these patterns illustrate that large herbivores play a key role in the assembly of plant communities and that trait- based assembly frameworks are an effective way to integrate the effects of herbivores.

Changes in Taxonomic Diversity

We found that herbivores did not influence the numbers of species in our system

(richness) but caused a shift in composition and structure. Herbivores may reduce competitive exclusion and increase species replacement, leading to increased species evenness and diversity. Through their role as disturbance agents, depositors of metabolic

15 wastes and consumers, herbivores appear to facilitate species coexistence by altering biotic interactions. Ecological models predict an increase in diversity at intermediate levels of disturbance as a result of reduction in competitive exclusion (Grime 1973).

Similarly, when stabilizing niche differences are greater than relative fitness differences, they foster diversity during community assembly by preventing competitive exclusion of inferior competitors by superior competitors (Chesson 2000; HilleRisLambers et al.

2012). Our results suggest that herbivores cause some species to more strongly limit themselves than others, which allow for species replacement. One explanation for this increase in species replacement may be that herbivores decrease the number and diversity of exotic annual grasses that germinate in fall and flower in spring (e.g. Holcus lanatus;

Ender et al. 2017), which are well known to suppress annual forb abundances by forming a dense layer of recalcitrant litter that inhibits forb germination (e.g., Pitt and Heady

1978, Levine and Rees 2004) thereby increasing species evenness and diversity.

Although species evenness and diversity increased overall, it was lowest in the coarsest soil formation, Sirdrak. The effect of herbivores combined with water stress due to increased drainage in coarse soils, likely periodically results in partial or total loss of plant organs. These pressures have likely selected for growth strategies that compensate for the effects of herbivores via rapid growth--rather than tolerating the effects of herbivores through prostrate growth (Diaz et al. 1997), thereby contributing to the shift in evenness and diversity. Here, herbivores did not have an effect on richness, which is likely due to species replacement and or the alteration of species dominance leading to similar values for plant species richness but differing composition. In a similar study, differences in plant diversity inside and outside enclosures were observed in several community types in the Serengeti (McNaughton 1983; Belsky 1986). They found that

16 diversity and evenness shifted but species richness was not significantly different.

McNaughton attributed this to replacement by tall species in ungrazed areas formerly dominated by short species when the area had been grazed. Although a taxonomic approach can describe changes in community composition, it cannot be linked to possible mechanisms causing such shifts; whereas with a functional approach, such inferences can be applied.

Changes in Community-weighted Traits

Using a functional approach, we found that the influence of herbivores has shifted functional strategies from a more stress avoidant strategy to a more resource acquisitive strategy as evidenced by an increase in values for traits associated with hydraulic capacity, stature and growth rate. A change in the CWM of a trait can indicate the assembly mechanism of habitat filtering (Catford, Jansson & Nilsson 2009). Because of our experimental design, we can determine with a higher degree of confidence that these shifts are likely created through a biotic filter where resource competition acts to constrain a community to certain traits values (Keddy 1992; Díaz et al. 1998; Maire et al.

2012) rather than through an abiotic filter (Weiher & Keddy 1995; Cornwell & Ackerly

2009; Lebrija-Trejos et al. 2010). Plants exhibit various strategies to survive such biotic restrictions, often leading to functional redundancy around an optimal trait value

(equalizing fitness processes). While some plant traits may shift to resist the effect of herbivores through tolerance, other plant traits may shift to resist through different mechanisms of avoidance (Rosenthal & Kotanen 1994). The tolerant strategy requires tissues efficient at acquiring resources to sustain regrowth, while the avoidant strategy needs conservative tissues to prevent plant consumption (Díaz et al. 2001; Cingolani,

Posse & Collantes 2005). Here, we predominantly find shifts in traits that suggest a tolerant, resource acquisitive strategy is employed to cope with the effects of herbivores

(e.g. greater dominance by plants that are able to capitalize and thrive on the disturbed environment and which invest less in long-lived structures).

We found a change in the CWM trait values for two of the five traits measured and a trend for an additional trait: decreasing stem-specific density (SSD), increasing height, and a trend for specific leaf area (SLA). Based on these trait responses, filtering may occur due to equalizing fitness differences. For example, the decreasing shift in SSD

(Figure 3a) indicates low stem density (with large vessels), leading to fast growth due to cheap volumetric construction costs and a large hydraulic capacity (Santiago et al. 2004,

Pérez-Harguindeguy et al. 2013). Here, herbivores shift the community to be dominated by species that possess traits suitable for the herbivore-modified habitat, such as species that are fast-growing which allow for quick recover after disturbance from herbivores.

This selection is also supported by the increasing CWM for height. Along with rapid growth, height is also associated with competitive vigor and provides further evidence for a shift toward a more resource acquisitive functional strategy. Furthermore, the increasing trend in SLA indicates the prevalence of species with relatively large, thin leaves. Together, the correlations between these traits support the plant economic spectrum (Wright et al. 2004; Freschet et al. 2010), indicating that large herbivores cause higher acquisition and turnover of resources in plants with increasing disturbance.

Changes in Functional Diversity

The contribution of a number of assembly processes can be inferred through the characterization of the functional diversity within a community, such as equalizing fitness differences (functional redundancy around an optimal trait), stabilizing niche differences, facilitation and limiting similarity. In our study, shifts in functional diversity have the potential to reveal biotic assembly mechanisms that herbivores may influence. Here, we find a clear functional response of plant communities to herbivores, as evidenced by shifts in functional diversity observed for four of our six traits. Plant communities were characterized by trait-specific and, in some cases, abrupt shifts between underdispersion and overdispersion due to the effects of herbivores and the heterogeneous environment.

There are a number of assembly mechanisms that can be inferred from these dispersion patterns, especially when single traits, rather than multivariate traits, are analyzed. For example, Weiher and Keddy (1995) found that limiting similarity may lead to trait overdispersion as a result of niche partitioning while environmental filtering may lead to trait underdispersion. We found increased functional redundancy (decreased functional diversity) for stem-specific density and leaf dry matter content, which are known to reflect a trade-off between growth potential and mortality risk from biomechanical or hydraulic failure. In this system, herbivores have decreased the range of values for stem growth and tissue longevity strategies indicating that species have converged toward an optimum trait value that favors a tolerance rather than an avoidance strategy. It can be inferred that herbivores may cause equalizing fitness differences to play a key role in structuring communities in this system.

In contrast, herbivores may simultaneously contribute to stabilizing niche differences. For functional diversity of height, we found context dependent outcomes;

19 herbivores caused traits to be overdispersed in the mixed and Sirdrak soil formations, underdispersed in Kehoe 2 and no effect in Kehoe 1. Depending on the underlying soil formation, the relative influence of elk on assembly mechanisms shifts. Furthermore, herbivores cause for multivariate functional diversity to increase, possibly indicating that community-wide niche partitioning may be occurring. Multivariate functional diversity was underdispersed in plot 1, located on Kehoe 2 soil formation, is fenced to exclude elk and is found on a ridgeline with high wind exposure in the northern most part of the experiment. We hypothesize that we did not detect additional plots exhibiting greater or lesser diversity than expected because both environmental and biotic filtering are likely to be occurring simultaneously.

Effects on Native and Exotic Species

Contrary to our expectations, the effect of herbivores on plant traits sometimes differs among native and exotic communities but many communities remained relatively functionally similar. In fact, our results indicate that the local environment may play a larger role in shifting percent cover of native verses exotic plant communities. It is possible that indirect effect of elk on the recipient microhabitat may contribute to such shifts. The concept of limiting similarity predicts that invasive species will be unlikely to establish if there are native species with similar traits present in the resident community or if available niches are filled. Several studies suggest that limiting similarity can confer invasion resistance and that communities with greater functional diversity are often less susceptible to invasion (Diaz & Cabido 2001; Fargione, Brown & Tilman 2003; Hooper et al. 2005). For example, in a California annual grassland, an invasive star thistle

(Centaurea solstitialis) had lower biomass in communities containing the functionally

20 similar native tarweed (Hemizonia congesta); both species are annual forbs and compete for late-season soil moisture (Dukes 2001). Further research examining redundancies among species are required to further determine the role of herbivores in this system.

Simultaneous Processes and Inferred Mechanisms

Overall, we found that herbivores had an effect on mechanisms that involve habitat-related constraints and biotic interactions (Keddy 1992; Cornwell et al. 2006) likely acting simultaneously (Spasojevic & Suding 2012). Such mechanisms can operate simultaneously because a restrictive environment can not only completely exclude species with less ideal traits, but also prevent species from achieving high abundance.

Similarly, competition can exclude species or, alternatively, keep less competitive species in low abundance. The way in which herbivores affect how assembly mechanisms are related is likely to have important consequences on which species (according to their traits) are completely filtered out of a given habitat and which ones are able to persist but not to dominate (Cingolani 2007). Unfortunately, we cannot entirely disentangle the mechanisms operating using functional diversity patterns because they require assumptions about what trait relates to what assembly process. This approach does, however, provide the opportunity to infer community assembly processes leading to a more quantitative understanding of such processes.

Conclusions

Most research on community assembly has focused on specific assembly rules and the influence of ecological mechanisms on the assembly process (Paine 1974,

Diamond 1975; Webb et al. 2002; Enquist 2002). Until now, the exploration of the influence of large mammalian herbivores on the process by which communities assemble

21 has received no explicit attention. Assessing the degree to which herbivores drive community assembly and functional traits has important implications: it provides insights into the mechanisms driving changes in plant communities and has the potential to allow perturbations in communities to be detected and mitigated. This study illustrates the importance of the effect of large herbivores on the relative influence of assembly processes on plant communities – and on native and exotic assemblages -- across heterogeneous landscapes. Our results indicate that herbivores can shift several processes, acting simultaneously, which can affect plant community assembly mechanisms and provide insights about the invasibility of the community.

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Table 1

Table 1. Results from ANOVA models evaluating the effects of tule elk and soil

formation (SF) on (a) species diversity, (b) species evenness, (c) species richness,

(d) percent cover of native species, and (e) percent cover of exotic species. Bold

text indicates significant results and italicized text indicates marginally significant

results.

Response Fixed effect DF F P (a) Diversity H’ Elk 1, 8 5.3112 0.0501 SF 3, 8 2.0582 0.1843 E x SF 3, 8 0.8529 0.5032

(b) Evenness Elk 1, 8 6.5370 0.0338 SF 3, 8 2.3467 0.1492 E x SF 3, 8 2.4352 0.1398

(d) Percent Cover Natives Elk 1, 8 2.5335 0.1501 SF 3, 8 4.5542 0.0384 E x SF 3, 8 0.3944 0.7606

(e) Percent Cover Exotics Elk 1, 8 2.0557 0.1895 SF 3, 8 3.5892 0.0659 E x SF 3, 8 0.2129 0.8847 (a) Evenness Elk 1, 8 6.5370 0.0338 SF 3, 8 2.3467 0.1492 E x SF 3, 8 2.4352 0.1398

Table 2

Table 2. Results from ANOVA models evaluating the effects of tule elk and soil

formation (SF) on (a) CWM SSD (log transformed), (b) CWM height (log

transformed), (c) CWM SLA (log transformed), (d) CWM LA (log transformed),

and (e) CWM LDMC (log transformed). Bold text indicates significant results and

italicized text indicates marginally significant results.

Response Fixed effect DF F P (a) CWM SSD Elk 1, 8 8.0387 0.0220 (log) SF 3, 8 0.3821 0.7688 E x SF 2, 8 0.8971 0.4836

(b) CWM height Elk 1, 8 10.677 0.0114 (log) SF 3, 8 4.9559 0.0313 E x SF 3, 8 3.4332 0.0724

(d) CWM LA Elk 1, 8 0.0110 0.9190 (log) SF 3, 8 1.0376 0.4266 E x SF 3, 8 0.5373 0.6698

(e) CWM LDMC Elk 1, 8 1.5168 0.2531 (log) SF 3, 8 8.3768 0.0075 E x SF 3, 8 1.0158 0.4350

Table 3

Table 3. Results from ANOVA models evaluating the effects of tule elk and soil

formation (SF) on (a) FDis Height, (b) FDis LDMC (log transformed), (c) FDis

SSD (log transformed), (d) FDis LA (log transformed), (e) FDis SLA, and (f)

Multivariate FDis. Bold text indicates significant results and italicized text

indicates marginally significant results.

Response Fixed effect DF F P (a) FDIS height Elk 1, 8 7.1401 0.0283 SF 3, 8 8.4222 0.0074 E x SF 3, 8 5.4912 0.0241

(b) FDis LDMC Elk 1, 8 6.3550 0.0358 (log) SF 3, 8 3.9365 0.0538 E x SF 3, 8 1.6579 0.2521

(d) FDis LA Elk 1, 8 0.1423 0.7158 (log) SF 3, 8 0.9064 0.4796 E x SF 3, 8 0.5936 0.6365

(e) FDis SLA Elk 1, 8 -0.7213. 0.4204 SF 3, 8 2.5214 0.1315 E x SF 3, 8 0.8718 0.4947

(f) Multivariate FDis Elk 1, 8 10.508 0.0118 SF 3, 8 0.8293 0.5141 E x SF 3, 8 3.7394 0.0603

Figure Legends

Figure 1. Mean ( +/- 1 S.E.) plant species diversity H’(a) , plant species evenness (b) and

plant species richness (c) as a function of elk (present or excluded) and soil

formation (ordered by soil texture from finest to coarsest: Kehoe variant 1, Kehoe

variant 2, mixed Kehoe variant 1/Sirdrak Sand, and Sirdrak Sand).

Figure 2. Mean (+/- 1 S.E.) percent cover native (a) and exotic (b) plant species per plot

as a function of elk and soil formation (ordered by soil texture from finest to

coarsest: Kehoe variant 1, Kehoe variant 2, mixed Kehoe variant 1/Sirdrak Sand,

and Sirdrak Sand).

Figure 3. Mean (+/- 1 S.E.) community weighted mean (CWM) of stem-specific density

(SSD) (a), CWM specific leaf area (SLA) (b), CWM height (c), CWM leaf area

(LA) (d) and CWM leaf dry matter content (LDMC) (e) as a function of elk and soil

formation (ordered by soil texture from finest to coarsest: Kehoe variant 1, Kehoe

variant 2, mixed Kehoe variant 1/Sirdrak Sand, and Sirdrak Sand).

Figure 4. Mean (+/- 1 S.E.) functional dispersion (FDis) of height (a), FDis leaf dry

matter content (LDMC) (b), FDis stem-specific density (SSD) (c), FDis leaf area

(LA) (d), FDis specific leaf area (SLA) (e) and multivariate FDis (f) as a function

of elk and soil formation (ordered by soil texture from finest to coarsest: Kehoe

variant 1, Kehoe variant 2, mixed Kehoe variant 1/Sirdrak Sand, and Sirdrak

Sand). Letters above bars correspond to the results from Tukey multiple

comparison tests.

Figure 1 Figure 1

3.5 Elk present A. Elk present Elk excluded Elk excluded 3

2.5

1.5 Species Diversity (H‘) Diversity Species

1 Kehoe 1 Kehoe 2 Mixed Sirdrak 0.9

0.8

0.7

0.6 Species Evenness Species

0.5 40 Kehoe 1 Kehoe 2 Mixed Sirdrak C.

30 25 20 15

10 Species Richness Species 5 0 Kehoe 1 Kehoe 2 Mixed Sirdrak

Soil Formation

Figure 2 Figure 2

80 A. Elk present 70 Elk excluded 60 50 40 30 20 10

Native Species % Cover % Species Native 0 Kehoe 1 Kehoe 2 Mixed Sirdrak 90 B. 80 Soil Formation 70 60 50 40 30 20

10 Exotic Species % Cover % Species Exotic 0 Kehoe 1 Kehoe 2 Mixed Sirdrak Soil Formation

Figure 3 Figure 3

1.4 A.

1.2

0.8

0.6 Elk present Elk excluded

0.4 Log CWM Log SSD 0.2

0 4.4 KehoeB. 1 Kehoe 2 Mixed Sirdrak 6 ab C.

4.2 Soil Formation b

5.4 4 a ab 3.8 4.8

3.6 4.2

3.4

Log CWM SLA CWM Log Log CWM Height CWM Log

3.6 3.2

3 3 3.2 Kehoe 1 Kehoe 2 Mixed Sirdrak 6 Kehoe 1 Kehoe 2 Mixed Sirdrak D. E. 2.8 Soil Formation a ab b 2.4 5.5 b 2 1.6 5

1.2 Log CWM LA CWM Log

0.8 4.5 Log CWM LDMC CWM Log 0.4 0 4 Kehoe 1 Kehoe 2 Mixed Sirdrak Kehoe 1 Kehoe 2 Mixed Sirdrak SoilSoil Formation Formation SoilSoil Formation Formation

Figure 4 Elk present 1.2 ab 1.2 Elk present Elk excluded Elk excluded A. a B. 1 abc abc 1 abc 0.8 abc 0.8 bc 0.6 c 0.6

0.4 0.4 FDIS Height FDIS

0.2 LDMC FDIS Log 0.2

0 0 0.8 Kehoe 1 Kehoe 2 Mixed Sirdrak Kehoe 1 Kehoe 2 Mixed Sirdrak C. 1.8 0.7 Soil Formation D. Soil Formation 1.5 0.6 0.5 1.2

0.4 0.9 0.3

0.6 Log FDIS LA FDIS Log

Log FDIS SSD FDIS Log 0.2

0.1 0.3 0 0 Kehoe 1 Kehoe 2 Mixed Sirdrak 1.2 0.16 F.Kehoe 1 Kehoe 2 Mixed Sirdrak E. Soil Formation 0.14 1 Soil Formation

0.12

0.8 0.1 0.6 0.08 0.06

FDIS SLA FDIS 0.4 0.04 0.2

Multivariate FDIS Multivariate 0.02 0 0 Kehoe 1 Kehoe 2 Mixed Sirdrak Kehoe 1 Kehoe 2 Mixed Sirdrak Soil Formation Soil Formation

Figure 4