If We Build It, Will They Come? Insect Communities As Indicators

IF WE BUILD IT, WILL THEY COME? INSECT COMMUNITIES AS INDICATORS

OF RESTORATION IN AN URBAN PRAIRIE NETWORK

Thesis

Submitted to

The College of Arts and Sciences of the

UNIVERSITY OF DAYTON

In Partial Fulfillment of the Requirements for

The Degree of

Master of Science in Biology

Amanda Nicole Finke

Dayton, OH

December 2019

IF WE BUILD IT, WILL THEY COME? INSECT COMMUNITIES AS INDICATORS

OF RESTORATION IN AN URBAN PRAIRIE NETWORK

Name: Finke, Amanda Nicole

APPROVED BY:

Chelse M. Prather, Ph.D. Faculty Advisor Assistant Professor Department of Biology

Karolyn Mueller Hansen, Ph.D. Committee Member Associate Professor Chair, Department of Biology

Ryan W. McEwan, Ph.D. Committee Member Associate Professor Department of Biology

Amanda Nicole Finke

2019

iii ABSTRACT

IF WE BUILD IT, WILL THEY COME? INSECT COMMUNITIES AS INDICATORS

OF RESTORATION IN AN URBAN PRAIRIE NETWORK

Name: Finke, Amanda Nicole University of Dayton

Advisor: Dr. Chelse M. Prather

The increasing negative effects of human impacts on the Earth have led to the urgent need for large-scale ecological restoration. One ecosystem of particular interest for restoration is tallgrass prairie, which only has 4% of its original 167 million acre range remaining in North America. However, restored and constructed prairies often do not support the same biodiversity and ecosystem services as remnant prairies. Many restoration projects only focus on reinstating vegetation, assuming that other trophic levels will colonize on their own. These higher trophic levels include arthropods, which make up a majority of the biodiversity in prairie ecosystems. We sought to determine if there is a difference in the insect communities in constructed and remnant prairies. It was hypothesized that insect communities would be different, with higher arthropod abundance and diversity in remnant sites, and older constructed sites would more closely resemble remnant sites. It is possible that indicator species of high-quality prairie could be identified, and that they may possess certain functional traits (morphological or life history) that allow them to colonize these sites. Sweepnet samples (100 sweeps per site) were taken at 5 old fields, 5 constructed prairies, and 5 remnant prairies in 2017, and 7

iv constructed prairies and 6 remnant prairies in 2018. All arthropods were then sorted to order, and some orders to morphospecies.

The only order of insects whose abundance was significantly different between habitat types was Coleoptera (p = 0.041), which were 3.5 times more abundant in remnant sites than constructed sites. The only family of Coleoptera whose abundance was significantly different between habitat types in 2017 was Phalacridae (p = 0.046) which were 7.6 times more abundant in remnant sites than constructed sites. The abundance of Phalacridae in constructed prairies increased with age since construction (p

= 0.03, R2 = 0.63; p = 0.09, R2 = 0.47). Ordinations of beetle families show that certain families are not being restored soon after the project, but rather restored slowly over long periods of time as late-successional species are able to colonize, such as Phalacridae.

These results could have large implications on how tallgrass prairies are restored and managed, and how these ecosystems should be assessed for restoration, specifically looking at other aspects of the ecosystem other than vegetation.

To my parents, for giving me the world.

Thank you for your endless love and support.

vi ACKNOWLEDGMENTS

First, I would like to express my immense gratitude to my advisor, Dr. Chelse

Prather. Thank you for your continuous support and encouragement, and for allowing me to turn an undergraduate research project into a master’s thesis. I would also like to thank my committee members, Drs. Ryan McEwan and Karolyn Hansen, for their helpful feedback and guidance throughout my entire time at UD.

Thanks to all of the park districts and land managers who allowed me to sample their prairies for this study, as well as Dave Nolin for sharing his extensive knowledge of

Ohio prairies.

Thank you to all of the Prather Lab members (past and present) who have helped me with this project, whether it was processing soil samples or just listening to me talk about beetles for what was probably an unreasonable amount of time. I appreciate each of you.

I would also like to thank the other graduate students, especially my fellow ecologists. Thank you for all of the coding sessions, Brown Bags, chats, and overall friendship.

Finally, a special thanks goes to the 2 people without whom I would not be here: my parents. To my dad, thank you for being my field assistant and driving all over southwest Ohio with me. To my mom, thank you for always proofreading my papers for me and for always being willing to talk. You both have given me every opportunity I could have ever asked for and have encouraged me to follow my dreams. Thank you for always believing in me even when I don’t believe in myself.

vii This research would not have been possible without funding from the University of Dayton Graduate Student Summer Fellowship and the noble sacrifice of thousands of insects.

viii PREFACE

“Here is the means to end the great extinction spasm. The next century

will, I believe, be the era of restoration in ecology.”

E. O. Wilson (1992)

Throughout our history, humans have had profound impacts on ecosystems across the globe. The ecosystems of the world have been changed more in the last half century than any other point in recorded human history, and nearly all ecosystems have been significantly altered by human activity (Millennium Ecosystem Assessment 2005). As our population has continued to grow at an exponential rate, much of the land on Earth was subsequently converted for human use (Houghton 1994). In the roughly 30 years it took for the human population to double from 2.5 billion to 5 billion, more land was converted for agriculture than the 150 years between 1700 and 1850 (Millennium

Ecosystem Assessment 2005). More than one-third of land on Earth has been converted for human use while at least another one-third has been heavily degraded by consequences of human use such as habitat fragmentation, invasions, and pollution

(Vitousek et al. 1997; Millennium Ecosystem Assessment 2005). In the past 100 years, humans have increased the species extinction rate by as much as 1,000 times the typical rates over Earth’s history, propelling us into the sixth mass extinction (Millennium

Ecosystem Assessment 2005; Jackson 2008; Barnosky et al. 2011; Pievani 2014;

Ceballos et al. 2015; McCallum 2015).

ix These negative anthropogenic effects are only projected to worsen as our populations continue to grow, and the effects of climate change become more severe

(Thomas et al. 2004). These changes have led to the urgent need for large-scale ecological restoration. Restoration is, of course, a meager second to the preservation of original ecosystems, and the ideal solution would be to avoid degradation in the first place. But with much of the planet already developed for human use, restoration remains one of the only options to keep these native ecosystems intact for generations to come.

x TABLE OF CONTENTS

ABSTRACT……………………………………………………………………………...iv

DEDICATION……………………………………………………………………………vi

ACKNOWLEDGMENTS…………………………………………………………….....vii

PREFACE………………………………………………………………………………...ix

LIST OF FIGURES...……………………………………………………………………xii

LIST OF TABLES………………………………………………………………..…….xiii

INTRODUCTION………………………………………………………………………...1

METHODS………………………………………………………………………………..6

RESULTS…………………………………………………………………………………9

DISCUSSION……………………………………………………………………………12

FIGURES………………………………………………………………………………...19

TABLES………………………………………………………………………………....29

REFERENCES…………………………………………………………………………..40

xi LIST OF FIGURES

Figure 1. Historic range of tallgrass prairie in the United States (left) and current range of tallgrass prairie in the United States (right)…………………………………….19

Figure 2. Counties sampled in this study shown in green (left) and all sites sampled are labelled and color coded based on habitat type (right)………………………………20

Figure 3. An example of each habitat type is shown…………………………………….21

Figure 4. Boxplot showing total abundance of arthropods in August 2017……………..22

Figure 5. Boxplot showing abundance of Coleoptera in August 2017…………………..23

Figure 6. Boxplot showing abundance of Phalacridae in August 2017………………….24

Figure 7. Linear regressions of abundance of Phalacridae and age since construction….25

Figure 8. Cluster analysis of 2017 insect order data………………………………………26

Figure 9. NMDS ordinations of beetle communities at each sampling period in 2018….27

xii

LIST OF TABLES

Table 1. List of sites sampled in this study including habitat type and location………...29

Table 2. Results from an ANOVA with Poisson distribution to determine differences between the 3 habitat types of 2017 insect order data………………………31

Table 3. Results from an ANOVA with Poisson distribution to determine differences between the 3 habitat types of 2017 beetle family data……………………..32

Table 4. Results from a repeated measures ANOVA with a Poisson distribution to determine differences between sampling periods and habitat types using 2018 beetle abundances………………………………………………………………………..33

Table 5. Results from a repeated measures ANOVA with a Poisson distribution to determine differences between sampling periods and habitat types using 2018

Phalacridae abundances………………………………………………………………….34

Table 6. Results of Indicator Species Analysis (ISA) of 2017 insect order data………...35

Table 7. Results of Indicator Species Analysis (ISA) of June 2018 beetle family data…36

Table 8. Results of Indicator Species Analysis (ISA) of July 2018 beetle family data….37

Table 9. Results of Indicator Species Analysis (ISA) of August 2018 beetle family data……………………………………………………………………………………….38

Table 10. Results of generalized linear models to determine what factors may be driving Coleoptera and Phalacridae abundances………………………………………...39

xiii INTRODUCTION

The loss of tallgrass prairie is considered by some to be the largest landscape change of any North American ecosystem (Larsen and Work 2003). Prior to European settlement, approximately 167 million acres of North America was covered by tallgrass prairie, occurring along the eastern Great Plains with a prairie peninsula radiating north and east into Indiana and Ohio (Samson and Knopf 1994; Samson et al. 2004). Since then, it is estimated that only 4% of its original range remains (Samson et al. 2004)

(Figure 1; Smith and Butler 2011). A majority of the prairie landscape was converted for agriculture due to the fertile soil, while other areas were developed into urban areas.

Portions of prairies were also lost to suppression of fire, introduction of invasive species, and overgrazing (Risser 1996; Hartnett et al. 1997; Samson et al. 2004). This transformation has significant implications as these prairies provided a multitude of ecosystem services that are beneficial to humans including erosion and flood control, nutrient cycling, enhancing watersheds, and carbon sequestration (Baer et al. 2002;

Polley et al. 2005; Olenick et al. 2005; Morton et al. 2010; Werling et al. 2014; Dias and

Belcher 2015). Due to its rapid depletion and an increased awareness of its ecological importance, tallgrass prairie has been the subject of many restoration projects over several decades.

While it has been shown that restoration can increase biodiversity and ecosystem services, restorations often do not reach levels of biodiversity and services found in remnant ecosystems (Benayas et al. 2009). Restoration ecology is still a relatively young discipline and has received its fair share of criticism. The most common criticism of

1 restoration is there are no established standards on how to set goals and evaluate success of restoration projects (Ruiz-Jaen and Aide 2005; Suding 2011; Prach et al. 2019). The most common goal of restoration projects is to reestablish an ecosystem’s diversity to that of a reference ecosystem, followed by goals to restore the functioning and stability of the ecosystem (Suding 2011; Hallett et al. 2013). These projects, however, often fail to set criteria for monitoring success and even fewer actually monitor the outcomes (Suding

2011). Without the knowledge that could be gained from previous restorations, many projects move forward annually without knowing what has and has not worked in the past.

In addition to difficulty in monitoring success, most restoration efforts focus only on reestablishing the plant community, assuming other taxa will follow. This practice has been coined the “Field of Dreams hypothesis”: if you build it (an ecosystem, specifically the vegetation), they (non-target organisms) will come (Palmer et al. 1997).

Although widely practiced, relatively few studies have experimentally tested this approach (Palmer et al. 1997; Sudduth et al. 2011; Cahall et al. 2013; Frick et al. 2014).

Due to this mindset, not much is known about the restoration of higher trophic levels.

However, these nontarget organisms, such as arthropods, fungi, and birds, provide important ecosystem services such as pollination, decomposition, and seed dispersal, respectively (Kremen et al. 1993; Young 2000; Andersen et al. 2004; Ward and Larivière

2004; Orlofske et al. 2011; Prather et al. 2013), making these organisms essential to creating a self-sustaining ecosystem. Therefore, an understanding of their restoration is needed to truly assess restoration efforts.

2 Despite making up a majority of the biodiversity of many ecosystems and providing essential services, insect communities in restorations have been greatly understudied. When insects have been assessed in restorations, it has been generally shown that insect abundances and diversity do not reach the levels of reference ecosystems (Bomar 2001; Shepherd and Debinski 2005; Kwaiser and Hendrix 2008;

Nemec and Bragg 2008; Orlofske et al. 2011; Rowe and Holland 2013).

Because of their high abundance and diversity, as well as representing key components in an ecosystem, insects have the possibility of being ideal indicator groups of a healthy ecosystem (Kremen et al. 1993; Brown 1991; Hodkinson and Jackson 2005;

Orlofske et al. 2010). The use of indicator groups could be a better estimate of the ecological value of a site rather than species diversity, which is the most commonly used criteria (Webb 1989; Cousins 1991; Dufrêne and Legendre 1997). Insects as indicators have been frequently used in aquatic ecosystems to monitor water quality, but have only gained momentum in terrestrial ecosystems in the last several decades (Holloway 1980;

Holloway and Stork 1991; McGeoch 1998). While native vegetation can be easily established, prairie-dependent arthropods are rarely relocated, and therefore may be useful for evaluating and monitoring prairie habitats (Orlofske et al. 2011).

A wide variety of arthropods have been suggested as indicator species, including orthopterans (Orlofske et al. 2010), leafhoppers (Orlofske et al. 2010; Rowe and Holland

2013), ants (Peck et al. 1998; Orlofske et al. 2010), crab spiders (Orlofske et al. 2010), dipterans (Orlofske et al. 2010), and collembola (Brand and Dunn 1998). Lepidoptera

(butterflies and moths) have been suggested as indicators because of their diversity, well known life history and taxonomy, ability to be readily identified, and their importance in

3 ecosystem functioning (Summerville et al. 2004). In prairie ecosystems, moth species most likely to be found in restored prairies were those that possess long flight periods, multivoltine life cycles, a preference for larval feeding on legumes, a mean smaller body size (~2.1 cm wingspan), and a large regional abundance (Summerville et al. 2006).

Coleoptera (beetles) have been identified as indicators in several ecosystems (stag beetles in beech-dominated forests: Lachat et al. 2012; ground beetles in tallgrass prairies:

Larsen et al. 2003, Barber et al. 2017; tiger beetles: Pearson and Cassola 1992). Studies focusing on ground beetle communities in prairies have found newly restored sites to be characterized by small, macropterous (larger wings), phytophagous (feeding on plants) species, while older sites contained larger species more likely to be flightless and carnivorous (Barber et al. 2017). These insect colonization patterns suggest that a functional trait approach could help to predict indicator groups.

In this study, we sought to determine if insect communities are being restored in tallgrass prairies of southwest Ohio by examining the communities present in remnant prairies and constructed prairies of varying ages. We addressed the following questions:

(1) is there a significant difference in insect communities in constructed and remnant prairies? (2) do insect communities in constructed prairies begin to resemble those in remnant prairies as time progresses? and (3) are there any indicator groups present in remnant prairies, and what functional traits might make them good indicators of high- quality prairie (or not)? It was hypothesized that there would be differences in the insect communities present in remnant and constructed prairies, since it has been shown that constructed ecosystems do not support the same levels of biodiversity as remnant ecosystems. We also hypothesized that specifically Lepidoptera and Coleoptera could be

4 used as possible indicator groups in prairies because they are some of the most speciose insect orders and have great importance to ecosystem functioning.

5 METHODS

2.1 Study Sites

This study was conducted in 4 counties of southwestern Ohio (Clark, Greene,

Miami, Montgomery). Historically, this portion of Ohio was covered in patches of tallgrass prairie, but these prairies have been severely depleted due to agriculture and urban development (Transeau 1935; Gordon 1969; Nolin 2018). Conservation and land management agencies are increasingly seeking to restore prairies in this area. With these constructions, along with the small remnant prairies remaining, this area is an ideal location to examine the functioning and diversity of natural and constructed prairie ecosystems.

A total of 17 sites were sampled over the course of two summers (2017, 2018)

(Table 1; Figure 2). We sampled in August 2017 to determine if the total number of arthropods or any particular insect orders were affected by habitat type. This sampling period included 14 sites divided into 3 different habitats (Figure 3). Four sites (Hebble

Creek, Karohl Park, Undisclosed, Germantown) were old fields, which are agricultural fields that had gone fallow and unmanaged (Figure 3, panel A). Five sites (Oakes

Quarry, Carriage Hill, Englewood, Sugarcreek, Possum Creek) were constructed prairies that were man-made (Figure 3, panel B). Five sites (Broadwing Prairie, Sand Ridge

Prairie, Stillwater Prairie Reserve, Goode Prairie Preserve, Huffman Prairie) were remnant prairies, which are naturally occurring prairies (Figure 3, panel C). In 2018, we looked at differences in arthropods over time by sampling 3 times over the summer, sampling at a total of 13 sites divided into 3 habitat types. Old fields were not sampled in

6 2018 because they did not provide any sufficient insight into restoration of insect communities. Two constructed prairies (Leadingham Prairie, Medlar Conservation Area) were added in 2018 to establish a chronosequence of age since construction. Constructed prairies were further divided by age into young constructions (6 – 15 years old) and old constructions (22 – 38 years old) to allow for analysis based on age. One remnant prairie

(Prairie Grass Trail) was added in 2018 to increase our sample size and allow for better analysis.

2.2 Data Collection

To measure the relative abundance and diversity of the insect communities of these prairies, I took sweepnet samples during each sampling period, with 4 sets of 25 sweeps per site (100 sweeps per site in each sampling period). I then pooled the samples for each site and sorted all individuals to order. Once sorted to order, I further sorted

Coleoptera (beetles) to family and morphospecies.

To determine how plant biomass and composition might affect insect composition, we sampled plants in August of 2017 and 2018. I conducted visual surveys to determine plant composition by randomly placing a 36-cm hoop and estimated percent cover of each plant species, as well as percent bare ground, percent grass, percent forb, and percent tree/shrub (4 hoops per site). I measured aboveground biomass by cutting all aboveground biomass (above 2-cm) within a 1-m x 10-cm area (4 per site). I then allowed these samples to dry for 48 hours (70º C) before weighing them.

I obtained soil characteristics for each site in August 2017 and 2018 by taking 5

10-cm soil cores at each site. I separated approximately half of each pooled sample and removed the roots. I weighed the roots and soil to obtain wet weights, and then allowed

7 the samples to dry for 48 hours (70º C) and weighed them to obtain dry weights. I used these measurements to calculate percent soil moisture, percent root moisture, and percent roots. I added 20 grams of soil to 20-mL of water and allowed the sample to stir for 10 minutes, then rest for 10 minutes. I used this sample to measure pH and conductivity.

2.3 Data Analysis

All statistical analyses were completed using R version 3.5.2, RStudio version

1.1.463, and SAS version 9.4. P-values less than 0.05 were considered to be significant.

For August 2017 data, I used analyses of variance (ANOVA) to determine differences between the 3 habitat types. Due to non-normal distributions, Poisson models were used. For 2018 data where I sampled 3 times over the summer, I used a repeated measures ANOVA (with Poisson distribution) for the insect community data to determine if there were any significant differences between sampling periods and between the 3 habitat types. Additionally, I used a correlation matrix to look for relationships between insect community data and possible explanatory variables (age of construction, soil characteristics, plant composition). This matrix was then used to conduct linear regressions and create generalized linear models. I used non-metric dimensional scaling

(NMDS) to determine similarity of insect communities between sites. I created a Bray-

Curtis dissimilarity matrix to quantify differences between sites, which was then used to perform a cluster analysis to group sites based on species composition. I conducted an indicator species analysis (ISA) to identify any group that was indicative of the habitat types.

8 RESULTS

3.1 Habitat type did not affect insect abundance, except for Coleopterans

Over all 4 sampling periods, 26,287 arthropods were sorted to order and 4,391

Coleopterans were sorted to family. Habitat type did not affect the total number of arthropods present at any sampling period (Figure 4; p = 0.68). In 2017, the only order of insects that was significantly different between habitat types was Coleoptera (Table 2;

Figure 5; p = 0.041) which were 3.5 times more abundant in remnant sites than constructed sites. The only family of Coleoptera that was significantly different between habitat types in 2017 was Phalacridae (Table 3; Figure 6; p = 0.046) which were 7.6 times more abundant in remnant sites than constructed sites.

3.2 Abundance of Phalacridae increased with age since restoration and beetle community composition in older constructed sites converged with remnant sites

In 2018, both Coleoptera and Phalacridae were significantly different between habitat types at all 3 sampling periods (p < 0.001 in all cases) (Table 4; Table 5), with both total Coleopterans and one family, Phalacridae, being most abundant in August.

There were also significant differences in abundance between sampling periods, and the interaction between habitat type and sampling periods (p < 0.001 in all cases) (Table 4;

Table 5). The age of the constructed prairie (years since restoration) significantly predicted the abundance of Phalacridae in July (Figure 7; p = 0.03, R2 = 0.63) and this relationship was near significant in August (Figure 7; p = 0.09, R2 = 0.47), with

Phalacridae abundance increasing with age.

9 A cluster analysis of the August 2017 order data showed remnant sites grouping together and constructed sites grouping together based on age (Figure 8). Ordinations of beetle families showed interesting relationships at each sampling period (Figure 9). In

June 2018, the centroids of all 3 prairie types overlapped with each other (Figure 9, panel

A; stress = 0.13). In July 2018, the centroids of all 3 prairie types were separated (Figure

9, panel B; stress = 0.15). In August 2018, the centroids of remnants and old constructions overlapped on top of Phalacridae, while the new constructions are made up primarily of Carabidae and Lampyridae (Figure 9, panel C; stress = 0.15).

An indicator species analysis (ISA) of insect orders of August 2017 data identified Coleoptera as indicators of remnant sites (Table 6; p = 0.015; indval = 0.62).

When ISAs of beetle families were conducted, 2 families were identified as indicators of newly constructed sites: Lampyridae in July (Table 8; p = 0.011; indval = 0.79) and

August (Table 9; p = 0.032; indval = 0.63), and Carabidae in August (Table 9; p = 0.007; indval = 0.91).

3.3 Abundance of Coleoptera and Phalacridae is predicted by plant biomass, percent forbs, and percent roots

The abundance of both Coleoptera and Phalacridae in these prairies was best predicted by biomass and percent forb in August 2017 (p = 0.02, R2 = 0.63; p = 0.0002,

R2 = 0.84) (Table 10). Higher abundances of Coleoptera and Phalacridae were present with higher plant biomass and a higher percentage of forbs. In August 2018, abundances of both Coleoptera and Phalacridae was best predicted by percent forb and percent roots in August 2018 (p = 0.07, R2 = 0.53; p = 0.07, R2 = 0.53) (Table 10). Higher abundances

10 of Coleoptera and Phalacridae were present at sites with higher percentages of forbs and roots.

11 DISCUSSION

“So important are the insects and other land-dwelling arthropods that if all

were to disappear, humanity probably could not last more than a few

months.”

E.O. Wilson (1992)

Even though insects have been said to be more important to ecosystem functioning than the larger vertebrates that are the subject of most conservation efforts

(Wilson 1987), there is still little known about their role in ecosystem restoration. The results of this thesis provide evidence that insects can be used as indicators of successful restoration in prairie ecosystems. The only insect order we were able to identify as indicators of remnant prairies was Coleoptera (beetles), with more beetles present in remnants than old fields, newly constructed prairies, and old constructed prairies. This trend seemed to be driven mostly by one particular family of beetles, Phalacridae, which were significantly more abundant in remnant prairies. The results from our NMDS suggest that beetle community composition is being restored, but it takes long periods of time, at least 30 years, for this to occur. This is supported by previous research showing that restorations could have a 30 – 50 year recovery period (Fuhlendorf et al. 2002).

4.1 Beetles as an indicator group of high-quality prairie

Beetles are considered to be the most taxonomically diverse order of animals, with over 350,000 species described worldwide (Wilson 1987; Gould 1993; Farrell 1998;

12 Oberprieler et al. 2007; Grove and Stork 2000; Zhang 2011; Zhang et al. 2018). Beetles also play important roles in ecosystem functioning, ranging across all trophic groups and providing essential ecosystem services such as pollination, decomposition, and seed dispersal (Kremen et al. 1993; Hutcheson et al. 1999; Young 2000; Andersen et al. 2004;

Ward and Larivière 2004; Orlofske et al. 2011). One of the most commonly used invertebrate indicators in the Northern Hemisphere is Carabidae (ground beetles) (Stork

1990; Eyre and Luff 2002; Andersen et al. 2004), and a majority of the studies in prairies focus only on ground beetles, and generally ignore the role of aboveground beetles

(Larsen et al. 2003, Barber et al. 2017). Studies that have examined aboveground insect communities have identified several beetle families as potential indicator species in prairies, including Phalacridae, Coccinellidae, Cantharidae, and Elateridae (Orlofske et al. 2010).

Aboveground beetles may make a good indicator group because of their large and diverse populations, their ease in sampling, distributions reflecting successional change, sensitivity to disturbance and ecosystem change, and reference collections can be inexpensively and easily maintained (Brown 1991; Stork and Samways 1995; Kremen et al. 1993; Hutcheson et al. 1999; Andersen et al. 2004). While there are several qualities which would make beetles a good indicator group, there are also some difficulties associated with beetles as indicators. While diversity can be an advantage in identifying indicator species (Brown 1991; Stork and Samways 1995; Hutcheson et al. 1999), this can also make them difficult to quickly identify, and there is a general lack of trained taxonomists (New 1998; Ward and Larivière 2004; Orlofske 2008). Additionally, many insect species, including beetles, remain undescribed (Wilson 1987). Like all insects,

13 beetles lack attention and support from the public, officials, and funding agencies, causing them to be left out of monitoring and management policies (Andersen et al. 2004;

Ward and Larivière 2004). There is also a severe lack of baseline data on aboveground beetles in prairies, which makes it difficult to monitor changes in their populations, and design restoration goals.

Generally, coleopteran abundance increased with plant biomass, percent forb, and percent roots. This result is intuitive given that many aboveground beetles are associated with consuming pollen, leaves, and other parts of prairie plants (Marshall 2018). Several species of beetles feed on different parts of plants at different stages of development. For example, many species of flea beetles feed on roots as larvae, but feed on leaves as adults.

4.2 Phalacridae as indicators of high-quality prairie

Phalacridae were more numerous in remnant prairies, with more present as age since construction increased. Phalacridae, also known as the shining flower or shining mold beetles, are one the most poorly known beetle families (Steiner 1984; Gimmel

2011a; Gimmel 2012). This family of beetles has been seemingly neglected due to its small size and monotonous appearance (Steiner 1984; Gimmel 2011a). Phalacrids typically are only able to be identified with close examination of the male genetalia

(Arnett 2002). Although poorly known, they have previously been identfied as possible indicator species in the tallgrass prairies of Iowa (Orlofske 2010), and now as promising candidates in southwest Ohio.

14 While a majority of Phalacrids are associated with fungi, Olibrus (the likely genus present in our field sites) are diurnal, flower-visiting pollen feeders as adults, while the larvae appear to feed on fluid material within flower heads (Gimmel 2011b). Olibrus is currently the largest genus in Phalacridae in terms of described species (Gimmel 2011b).

Members of the plant family Asteraceae (including Solidago, Symphyotrichum, Achillea, and Chrysopsis) are the only known hosts of larval Olibrus (Arnett 2002; Gimmel

2011b). It was shown that Phalacridae abundance increased with an increased biomass and percentage of forbs. Because asters are a type of forb, their increased presence in prairies could explain an increase in abundance of Phalacridae.

In order for Phalacrids to be a good indicator group, they need to be more extensively studied. The life histories of most Phalacridae are entirely unknown. Host plants for both larval and adult stages are for the most part unknown. Knowing what plants need to be present for these beetles to persist could be vital in ensuring their establishment in newly constructed prairies. Another issue with the current knowledge of

Phalacridae is there is very few individuals who are able to identify them to species. An important aspect of an indicator species is to be readily identifiable. While Phalacridae are readily identifiable to family, they are incredibly difficult to identify to species.

In the future, a functional trait approach may help to determine what about these beetles allow them to colonize sites in the way they have been shown to colonize in this study. We expect that beetles present in remnant prairies, like Phalacridae, would have smaller wings, smaller or fewer broods per season, and have a more specialized diet.

Beetles that would be able to colonize newly constructed prairies would be expected to have larger wings that would allow them to travel longer distances, have large and

15 numerous broods per season, and be generalists, feeding on weeds and grasses which would be the first vegetation to be present in a newly constructed site.

4.3 Lampyridae and Carabidae as indicators of newly constructed prairie

Lampyrids (fireflies) are typically found in more disturbed habitats, such as old fields. Larvae eat snails, slugs, and worms, while adults can eat other Lampyrids, pollen, nectar, or do not feed as adults (Marshall 2018). Lampyrids were more abundant in constructed sites, which also typically had the greatest abundances of Mollusca, which would provide plenty of food for the larvae.

Carabids (ground beetles) have been shown to be indicators of high-quality prairie in other studies (Larsen et al. 2003, Barber et al. 2017). In our study, ground beetles were collected at younger constructed sites. However, the methodology used for collecting insects in this study was not ideal for collecting ground beetles. Ground beetles are typically not active during the day, spending their time hiding under debris, and rarely fly due to their reduced wings. Because of their behavior, the proper method for sampling ground beetles is through pitfall sampling, which allows the beetles to fall into the trap while crawling on the ground and be captured. These traps are also left out for at least 48 hours, which would take into account the most active periods for ground beetles, while sweepnetting has to be done during their less active periods. Our results are not the most reliable in identifying ground beetles as indicators of a newly constructed habitat due to our sampling technique. The sites where ground beetles were collected typically had low plant biomass. With short and thin vegetation, sweeps may have been closer to the ground, which could account for Carabids being collected via sweepnetting at those sites.

4.4 Increased importance of understanding restoration

Understanding restoration becomes increasingly important as it becomes a necessary strategy in mitigating human effects on ecosystems. Several large-scale initiatives and agreements have been launched at the global scale that promote restoration

(Gaan et al. 2019). These initiatives include: the United Nations (UN) Sustainable

Development Goals (calls for restoration of marine and coastal ecosystems, as well as terrestrial ecosystems), the UN General Assembly Decade on Ecosystem Restoration

(2021 – 2030), the Convention on Biological Diversity (goal of restoring 15% of degraded ecosystems by 2020 and views ecological restoration as key to delivering essential ecosystem services), and the Intergovernmental Science-Policy Platform on

Biodiversity and Ecosystem Services (restoration viewed as a key element needed to avert mass extinctions and the subsequent loss of ecosystem services) (Gaan et al. 2019).

However, without understanding the outcome of previous restoration projects, we may be proceeding with strategies that are less successful in creating functioning ecosystems.

This study shows that insect communities play crucial roles in helping managers evaluate restoration efforts. Insect abundances can be easily monitored and measured, which is an important aspect of a good indicator group. While some insects require a bit more specialized knowledge to identify, managers and technicians could be easily trained in insect identification. Restoration projects are known to be highly variable at the beginning, so continuous monitoring of the insect community could detect early warning signs that the project may not be going as desired. Also, as this study has shown, full recovery can take longer than the time frame that restoration projects are typically

17 monitored (Matthews et al. 2009). While this study has shown the importance of beetle communities in particular in evaluating restoration efforts, more studies need to be done on the functional traits of prairie insects within the context of restoration to determine what may hinder some species from colonizing at earlier time periods, and which species may best indicate successful restorations in comparison to reference ecosystems. This type of understanding could ultimately lead managers to better managing for the restoration of insect communities instead of solely focusing on plant communities.

18 FIGURES

Figure 1: Historic range of tallgrass prairie in the United States (left) and current range of tallgrass prairie in the United States (right).

Adapted from Smith and Butler 2011.

Figure 2: Counties sampled in this study shown in green (left) and all sites sampled are labelled and color coded based on habitat type

(right). Old fields are shown in white, constructed sites are shown in black, and remnant sites are shown in green.

Figure 3: An example of each habitat type is shown. Panel A shows an old field (Hebble Creek). Panel B shows a constructed site

(Englewood). Panel C shows a remnant site (Huffman Prairie).

Figure 4: Boxplot showing total abundance of arthropods in August 2017. There was no significant difference in arthropod abundance in the different prairie types (p = 0.68).

Figure 5: Boxplot showing abundance of Coleoptera in August 2017. Abundance of

Coleoptera was significantly higher in remnant sites than in constructed sites (p = 0.041).

Figure 6: Boxplot showing abundance of Phalacridae in August 2017. Abundance of

Phalacridae was higher in remnant sites than constructed sites, but these results were not significant (p = 0.046).

24 A B C

p = 0.12 p = 0.03 p = 0.09 R2 = 0.41 R2 = 0.63 R2 = 0.47

Figure 7: Linear regressions of abundance of Phalacridae and age since construction. This relationship was significant in both July

(p = 0.03, R2 = 0.63) and August (p = 0.09, R2 = 0.47).

CP Measure of Dissimilarity of Measure OF RP RP CP OF CP OF OF CP RP RP CP

Figure 8: Cluster analysis of 2017 insect order data. Old fields are signified by OF, constructed sites by CP, and remnant sites by RP.

Remnant sites are grouped together on the right, and constructed sites are grouped together based on age (Oakes Quarry and Carriage

Hill – young constructions; Englewood, Possum Creek, Sugarcreek – old constructions).

26 A B C

Figure 9: NMDS ordinations of beetle communities at each sampling period in 2018. Panel A (June) shows all 3 habitat types overlapping (stress = 0.13). Panel B (July) shows all 3 habitat types separating from each other (stress = 0.15), indicating differences

27 in beetle community composition. Panel C (August) shows remnant and old constructions converging on Phalacridae, while the beetle communities of new constructions are driven more by Carabidae and Lampyridae (stress = 0.15).

28 TABLES

Table 1: List of sites sampled in this study including habitat type and location.

Site Name Site Code Habitat Type Age (as of 2018) Location Sampling Periods

Hebble Creek HC Old Field - 39.830727, -84.00243 Aug 2017

Undisclosed UD Old Field - - Aug 2017

Karohl Park KP Old Field - 39.740693, -84.04025 Aug 2017

Germantown GT Old Field - 39.647128, -84.415845 Aug 2017

Leadingham Prairie LP Constructed 6 39.877786, -83.999432 Jun, Jul, Aug 2018

Medlar Conservation Area MCA Constructed 6 39.603960, -84.258753 Jun, Jul, Aug 2018

Oakes Quarry OQ Constructed 15 39.817653, -83.993949 Aug 2017; Jun, Jul, Aug 2018

Carriage Hill CH Constructed 22 39.879942, -84.094800 Aug 2017; Jun, Jul, Aug 2018

Englewood EW Constructed 25 39.867591, -84.269053 Aug 2017; Jun, Jul, Aug 2018

Sugarcreek SC Constructed 33 39.617715, -84.092614 Aug 2017; Jun, Jul, Aug 2018

Possum Creek PC Constructed 38 39.713117, -84.265426 Aug 2017; Jun, Jul, Aug 2018

Prairie Grass Trail PGT Remnant - 39.7888, -83.7130 Jun, Jul, Aug 2018

Broadwing Prairie BP Remnant - 39.643028, -84.413313 Aug 2017; Jun, Jul, Aug 2018

Sand Ridge Prairie SR Remnant - 39.716369, -84.210578 Aug 2017; Jun, Jul, Aug 2018

Stillwater Prairie Reserve SW Remnant - 40.156469, -84.392472 Aug 2017; Jun, Jul, Aug 2018

Goode Prairie Preserve GP Remnant - 40.167111, -84.404563 Aug 2017; Jun, Jul, Aug 2018

Huffman Prairie HP Remnant - 39.807224, -84.059347 Aug 2017; Jun, Jul, Aug 2018

30 Table 2: Results from an ANOVA with Poisson distribution to determine differences between the 3 habitat types of 2017 insect order data. Results that have been bolded are significant. The only insect order that was significantly different between habitat types was

Coleoptera (beetles).

Insect Order df F Significance

Acari 2 0.292 0.752

Araneae 2 0.750 0.495

Coleoptera 2 4.341 0.041 *

Diptera 2 1.569 0.252

Hymenoptera 2 0.909 0.431

Isopoda 2 0.884 0.441

Lepidoptera 2 1.362 0.296

Mantodea 2 2.008 0.181

Neuroptera 2 0.884 0.441

Odonata 2 1.148 0.352

Orthoptera 2 0.369 0.700

31 Table 3: Results from an ANOVA with Poisson distribution to determine differences between the 3 habitat types of 2017 beetle family data. Results that have been bolded are significant. The only beetle family that was significantly different between habitat types was Phalacridae (shining flower beetles).

Beetle Family df F Significance

Brentidae 2 0.655 0.538

Cantharidae 2 0.884 0.441

Cerambycidae 2 0.393 0.684

Chrysomelidae 2 0.347 0.715

Coccinellidae 2 2.357 0.141

Curculionidae 2 1.248 0.325

Lampyridae 2 0.422 0.666

Mordellidae 2 1.037 0.387

Phalacridae 2 4.089 0.046 *

Scarabaeidae 2 0.268 0.770

Scraptiidae 2 1.263 0.321

32 Table 4: Results from a repeated measures ANOVA with a Poisson distribution to determine differences between sampling periods and habitat types using 2018 beetle abundances. Results that have been bolded are significant.

Source Wald Chi-Square df Significance

(Intercept) 43927.936 1 > 0.0001 *

Type 158.136 2 > 0.0001 *

Time 184.227 2 > 0.0001 *

Type * Time 410.730 3 > 0.0001 *

33 Table 5: Results from a repeated measures ANOVA with a Poisson distribution to determine differences between sampling periods and habitat types using 2018 Phalacridae abundances. Results that have been bolded are significant.

Source Wald Chi-Square df Significance

(Intercept) 315.264 1 > 0.0001 *

Type 21.385 2 > 0.0001 *

Time 287.585 2 > 0.0001 *

Type * Time 116.540 3 > 0.0001 *

34 Table 6: Results of Indicator Species Analysis (ISA) of 2017 insect order data. Results that have been bolded are significant. The only significant indicator we were able to identify was Coleoptera (beetles). Coleopterans were more abundant in remnant sites.

Relative Abundance Indicator Value p val indval OF C R OF C R Acari 0.75 0.42 0.42 0.37 0.21 0.42 0.37 0.16 Araneae 0.36 0.46 0.46 0.29 0.24 0.46 0.29 0.24 Coleoptera 0.023 0.62 0.22 0.16 0.62 0.22 0.16 0.62 Diptera 0.16 0.47 0.47 0.26 0.27 0.47 0.26 0.27 Hemiptera 0.32 0.48 0.36 0.48 0.16 0.36 0.48 0.16 Hymenoptera 0.45 0.49 0.49 0.26 0.25 0.49 0.26 0.25 Lepidoptera 0.19 0.50 0.50 0.30 0.20 0.50 0.18 0.16 Mantodea 0.21 0.46 0.61 0.29 0.10 0.46 0.12 0.02 Neuroptera 1.0 0.20 0.0 1.0 0.0 0.0 0.20 0.0 Odonata 0.72 0.25 0.38 0.62 0.0 0.10 0.25 0.0 Orthoptera 0.64 0.43 0.31 0.26 0.43 0.31 0.26 0.43

35 Table 7: Results of Indicator Species Analysis (ISA) of June 2018 beetle family data. No family was found to be a significant indicator.

Relative Abundance Indicator Value p val indval NC OC R NC OC R Brentidae 0.85 0.25 0.33 0.33 0.33 0.22 0.25 0.11 Cantharidae 0.61 0.34 0.51 0.19 0.30 0.34 0.10 0.15 Carabidae 0.34 0.33 0.0 0.0 1.0 0.0 0.0 0.33 Cerambycidae 1.0 0.11 0.0 0.43 0.57 0.0 0.11 0.10 Chrysomelidae 0.90 0.38 0.29 0.33 0.38 0.29 0.33 0.38 Cleridae 0.69 0.21 0.15 0.23 0.62 0.05 0.06 0.21 Coccinellidae 0.42 0.45 0.27 0.60 0.13 0.09 0.45 0.07 Curculionidae 0.61 0.65 0.29 0.06 0.65 0.29 0.04 0.65 Erotylidae 1.0 0.15 0.0 0.60 0.40 0.0 0.15 0.07 Lampyridae 0.13 0.65 0.03 0.65 0.32 0.01 0.65 0.27 Melandryidae 1.0 0.15 0.44 0.33 0.22 0.15 0.08 0.04 Melyridae 0.26 0.33 1.0 0.0 0.0 0.33 0.0 0.0 Mordellidae 0.26 0.46 0.46 0.17 0.37 0.46 0.13 0.37 Mycetophagidae 0.20 0.33 1.0 0.0 0.0 0.33 0.0 0.0 Phalacridae 0.19 0.50 0.0 0.67 0.33 0.0 0.50 0.22

36 Table 8: Results of Indicator Species Analysis (ISA) of July 2018 beetle family data. Results that have been bolded are significant.

The only significant indicator we were able to identify was Lampyridae (fireflies). Lampyrids were more abundant in old constructed sites.

Relative Abundance Indicator Value p val indval NC OC R NC OC R Attelabidae 0.66 0.23 0.0 0.92 0.08 0.0 0.23 0.01 Brentidae 0.39 0.40 0.0 0.19 0.81 0.0 0.05 0.40 Cantharidae 1.0 0.17 0.0 0.0 1.0 0.0 0.0 0.17 Carabidae 0.52 0.25 0.0 1.0 0.0 0.0 0.25 0.0 Cerambycidae 1.0 0.17 0.0 0.0 1.0 0.0 0.0 0.17 Chrysomelidae 0.09 0.53 0.22 0.53 0.25 0.22 0.53 0.25 Coccinellidae 0.36 0.52 0.77 0.10 0.13 0.52 0.05 0.06 Curculionidae 0.59 0.36 0.47 0.10 0.43 0.16 0.02 0.36 Elateridae 0.23 0.33 1.0 0.0 0.0 0.33 0.0 0.0 Lampyridae 0.01 0.79 0.0 0.79 0.21 0.0 0.79 0.07 Meloidae 1.0 0.17 0.0 0.0 1.0 0.0 0.0 0.17 Mordellidae 0.73 0.32 0.30 0.22 0.48 0.30 0.06 0.32 Mycetophagidae 0.15 0.50 0.0 0.0 1.0 0.0 0.0 0.50 Phalacridae 0.62 0.37 0.12 0.74 0.14 0.08 0.37 0.09 Scarabaeidae 0.10 0.66 0.0 0.22 0.78 0.0 0.22 0.66

37 Table 9: Results of Indicator Species Analysis (ISA) of August 2018 beetle family data. Results that have been bolded are significant. The only significant indicators we were able to identify were Carabidae (ground beetles) and Lampyridae (fireflies). Both families were more abundant in newly constructed prairies.

Relative Abundance Indicator Value p val indval NC OC R NC OC R Anthribidae 0.62 0.26 0.0 0.21 0.79 0.0 0.05 0.26 Attelabidae 0.74 0.23 0.0 0.90 0.10 0.0 0.23 0.03 Brentidae 0.64 0.44 0.05 0.29 0.67 0.02 0.22 0.44 Carabidae 0.01 0.91 0.91 0.0 0.09 0.91 0.0 0.02 Cerambycidae 0.54 0.25 0.0 1.0 0.0 0.0 0.25 0.0 Chrysomelidae 0.31 0.47 0.16 0.37 0.47 0.16 0.37 0.47 Coccinellidae 0.92 0.15 0.44 0.33 0.22 0.15 0.08 0.07 Curculionidae 0.38 0.58 0.88 0.04 0.08 0.58 0.02 0.05 Lampyridae 0.04 0.63 0.94 0.0 0.06 0.63 0.0 0.01 Meloidae 1.0 0.17 0.0 0.0 1.0 0.0 0.0 0.17 Mordellidae 0.54 0.22 0.67 0.0 0.33 0.22 0.0 0.06 Mycetophagidae 0.24 0.33 1.0 0.0 0.0 0.33 0.0 0.0 Phalacridae 0.25 0.81 0.07 0.12 0.81 0.07 0.12 0.81 Scarabaeidae 0.37 0.40 0.0 0.21 0.79 0.0 0.10 0.40 Staphylinidae 1.0 0.17 0.0 0.0 1.0 0.0 0.0 0.17

38 Table 10: Results of generalized linear models to determine what factors may be driving Coleoptera and Phalacridae abundances.

Only significant results are shown.

p - value R2 Coleoptera Biomass and Percent Forb 0.015 0.63 Phalacridae Biomass and Percent Forb 0.00025 0.84 Coleoptera Percent Forb and Percent Root 0.045 0.57 Phalacridae Percent Forb and Percent Root 0.067 0.53

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