The Influence of Prairie Restoration on Hemiptera

CAN THE ONE TRUE BUG BE THE ONE TRUE ANSWER? THE INFLUENCE OF

PRAIRIE RESTORATION ON HEMIPTERA COMPOSITION

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

Stephanie Kay Gunter, B.A.

Dayton, Ohio

August 2021

CAN THE ONE TRUE BUG BE THE ONE TRUE ANSWER? THE INFLUENCE OF

PRAIRIE RESTORATION ON HEMIPTERA COMPOSITION

Name: Gunter, Stephanie Kay

APPROVED BY:

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

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

Mark G. Nielsen Ph.D. Committee Member Associate Professor Department of Biology

Stephanie Kay Gunter

2021

iii ABSTRACT

CAN THE ONE TRUE BUG BE THE ONE TRUE ANSWER? THE INFLUENCE OF

PRAIRIE RESTORATION ON HEMIPTERA COMPOSITION

Name: Gunter, Stephanie Kay University of Dayton

Advisor: Dr. Chelse M. Prather

Ohio historically hosted a patchwork of tallgrass prairies, which provided habitat for native species and prevented erosion. As these vulnerable habitats have declined in the last 200 years due to increased human land use, restorations of these ecosystems have increased, and it is important to evaluate their success. The Hemiptera (true bugs) are an abundant and varied order of insects including leafhoppers, aphids, cicadas, stink bugs, and more. They play important roles in grassland ecosystems, feeding on plant sap and providing prey to predators. Hemipteran abundance and composition can respond to grassland restorations, age of restoration, and size and isolation of habitat. I investigated the effects of these variables on the abundance and composition of Hemiptera within 13

Ohio prairies in order to answer 4 questions regarding prairie restoration: Do older constructed prairies resemble remnant prairies in hemipteran abundance, diversity, and composition more than they resemble newer constructed prairies? Does the size of a prairie fragment affect the abundance, diversity, and composition of Hemiptera? Does the distance of a prairie to an agricultural field affect the abundance, diversity, and composition of Hemiptera? Do any hemipteran morphospecies indicate particular prairie types? Insect samples were taken via sweep net from 13 prairies (6 remnant, 4 old

iv constructed, 3 new constructed) in 4 southwestern Ohio counties in summer 2019, and were sorted to order. I then sorted hemipterans to family and morphospecies, and analyzed their abundance and composition.

I found no significant difference in hemipteran abundance or number of families/morphospecies between remnant, old constructed, and new constructed prairies in summer 2019. However, in July 2019, remnant prairies had a significantly higher hemipteran diversity than old and new constructed prairies. In August 2019, NMDS ordination showed that hemipteran morphospecies composition in new constructed prairies diverged from remnant and old constructed prairies. These results suggest that while the hemipteran community is largely similar across remnant and constructed prairies in this system early in the summer, the communities begin to diverge as the growing season progresses. Additionally, in June 2019, two morphospecies (Miridae:

Lygus lineolaris and Psyllidae: Craspedolepta sp.) had a significant negative relationship with age of constructed prairie, and another morphospecies, Membracidae: Micrutalis calva was an indicator of remnant prairies. Finally, in July 2019, the family Membracidae increased in abundance as distance to agriculture increased. The relationships seen within these hemipteran families suggest that constructed prairies may need more maintenance over time to better replicate the conditions of remnant prairies, and that close proximity to agriculture may be limiting the potential of all prairies in this region.

To my parents, especially to my mother, who could not be here to see this. As I sit here

deciding what to write, she would tell me “three, two, one, decide!”

vi ACKNOWLEDGEMENTS

I would like to give a special thanks first and foremost to my advisor, Chelse

Prather, for her patience and guidance these past couple years. Thank you for giving me a chance, helping me to become a better researcher, and encouraging me to try my own way of doing things! Thank you also to my committee members Ryan McEwan and Mark

Nielsen for their feedback and support!

I would also like to thank the UD Biology Department, for providing support for graduate students during this unusual year. Thanks to the efforts of those in charge of our department, we were able to continue our research and stay on as TAs even as the campus shut down.

Thanks to the undergraduate members of the Insect Ecology Lab, for their tireless efforts helping to collect and sort insects! Also, thank you to my fellow graduate students in the lab, for their advice and good company- especially to Amanda Finke for providing a lot of help with R!

Thank you to the land managers who maintain the prairies that were used in this study for allowing us to sample there. And, thank you to the countless insects who were used in this experiment- many people do not realize how beautiful they are when viewed up close.

Finally, thank you to my friends and family, for always being there for me. My dad has been a great source of support always, and my mom would have been, too.

vii TABLE OF CONTENTS

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

DEDICATION………………………………………………………………………...vi

ACKNOWLEDGMENTS……………………………………………………………vii

LIST OF FIGURES..……………………………………………………………...…..ix

LIST OF TABLES ………………………………………………………………...... xi

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

METHODS…………………………………………………………………………...... 5

RESULTS…………………………………………………………………………...... 8

DISCUSSION………………………………………………………………………....10

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

TABLES ………………………………………………………………………….…..36

REFERENCES..……………………………………………………………………....41

viii LIST OF FIGURES

Figure 1. Representative images of the three prairie types used in this study…………...19

Figure 2. Box and whisker plots showing the total Hemiptera sampled at

each prairie type in each month of summer 2019…………..……………………20

Figure 3. Box and whisker plots showing the number of hemipteran

families sampled at each prairie type in each month of summer 2019…………..21

Figure 4. Box and whisker plots showing the number of hemipteran morphospecies

sampled at each prairie type in each month of summer 2019..…………………..22

Figure 5. Linear models showing the relationship between total Hemiptera

and age of constructed prairie in each month of summer 2019..……………...…23

Figure 6. Linear models showing the relationship between number of

hemipteran families and age of constructed prairie in each month of summer

2019……………………………………………………………………………....24

Figure 7. Linear models showing the relationship between number of hemipteran

morphospecies and age of constructed prairie in each month of summer 2019…25

Figure 8. Linear models showing the relationship between Simpson’s Diversity

Index and age of constructed prairie in each month of summer 2019…...... ….26

Figure 9. Box and whisker plots showing the abundance of Psyllidae

(jumping plant lice) across the 3 prairie types in June 2019.…...………………..27

Figure 10. Linear model showing the relationship between the abundance

of 2 hemipteran families and age of constructed prairie in June 2019..…....……28

ix Figure 11. Linear model showing the relationship between the abundance

of 2 hemipteran morphospecies and age of constructed prairie in June 2019...... 29

Figure 12. Box and whisker plots showing the difference in abundance of 2

hemipteran morphospecies between the 3 prairie types in June 2019....…...... …30

Figure 13. Box and whisker plot showing the difference in Simpson’s Diversity

Index between the three prairie types in July 2019.....…...……..……………..…31

Figure 14. NMDS showing the composition of 21 abundant hemipteran

morphospecies (those that make up >1% of the entire dataset) in June 2019...... 32

Figure 15. NMDS showing the composition of 21 abundant hemipteran

morphospecies (those that make up >1% of the entire dataset) in July 2019...... 33

Figure 16. NMDS showing the composition of 21 abundant hemipteran

morphospecies (those that make up >1% of the entire dataset) in August 2019...34

Figure 17. Linear model showing the relationship between the abundance of

Membracidae and distance to agriculture July 2019...... ……...……………….…35

x LIST OF TABLES

Table 1. Information about all prairies sampled in this study………………………...….36

Table 2. Total specimens collected of each Hemiptera family in summer 2019………...37

Table 3. Table showing results of linear regressions on the relationship

between size of prairie and total Hemiptera and number of families…………....38

Table 4. Table showing results of linear regressions on the relationship

between distance of prairie to agriculture and total Hemiptera and number of

families…….……………………………………………………………………..39

Table 5. Table showing indicator analysis output for Micrutalis calva in July 2019…....40

xi INTRODUCTION

The composition and distribution of ecosystems worldwide have changed dramatically in the last few centuries, as humans have converted an increasing amount of natural land for our purposes. Nearly all of Earth’s biomes have been severely affected by human activity, and temperate grasslands are among those most degraded (Millennium

Ecosystem Assessment 2005). The tallgrass prairie was historically one of the major biomes in the U.S., spanning 162 million ha prior to European settlement (Samson and

Knopf 1994). However, the range of tallgrass prairie has declined anywhere between 82-

99% since 1830 (Klopatek et al. 1979; Samson and Knopf 1994). This decline has decreased habitat for a variety of native species, led to increasing encroachment of prairies by forest-edge species, and increased soil erosion (Knopf 1986; Samson and

Knopf 1994). While prairie is not the primary habitat in Ohio, the state has historically been sprinkled with tallgrass prairie patches (Transeau 1935), and in southwest Ohio, organizations like the Five River Metroparks system have been restoring old agricultural fields into prairies and maintaining restored and native prairie remnant sites (Five Rivers

Metroparks 2021).

With many restorations in progress in southwest Ohio, it is important to learn if restored prairies in this area are beginning to resemble native remnant prairies to evaluate if restorations have been successful. Many evaluations of restoration projects focus first on the plant community (79%), while a smaller number study higher trophic levels (Ruiz-

Jaen and Aide 2005). However, even when a plant community appears to be fully restored, the community of arthropods might not reflect this (Longcore 2003). Despite

1 this, a smaller proportion of studies (35%) measure arthropod species richness to evaluate restorations (Ruiz-Jaen and Aide 2005). Arthropods such as insects are a wildly important taxonomic group for measuring restoration success because they provide or influence numerous ecosystem services, including pollination, decomposition, and nutrient cycling (Holl 1995; Tian, et al. 1997; Ruiz-Jaen and Aide 2005).

However, insects are not always able to colonize restored habitats due to isolation and limited dispersal abilities (Panzer 1988; Bomar 2001). There is often an assumption that higher trophic levels, like insects, will re-colonize a habitat once the plant community has been restored (Suding et al. 2004), but this this must be better tested in prairie restoration projects (Panzer 1988; Dobson et al. 1997; Bomar 2001). Many prairie specialist insects may have difficulty dispersing the distances needed to travel between highly fragmented prairies (Ehrlich 1961; Panzer 1988). This concern is highly relevant to prairie restorations in Ohio, due to their patchy distribution and small fragment size.

One order of insects that has been shown to be of importance in evaluation of grassland restorations is the Hemiptera, or true bugs (Biedermann 2002; Nemec and

Bragg 2008; Keene et al. 2020). Hemiptera are primarily sap consumers and thus occupy a unique functional role compared to other insect herbivores (Biedermann et al. 2005).

One study (Nemec and Bragg 2008) sampled both Hemiptera and Orthoptera

(grasshoppers) at restored and remnant tallgrass prairies in Nebraska, and found that while two families of orthopterans had greater diversity in remnant prairies, three families of hemipterans actually had greater diversity at restored sites. The authors link these differing responses to the presence of preferred host plants, which were distributed unevenly between prairie types. This finding illustrates that orthopterans, despite being

2 commonly used in studies of conservation and restoration (Chambers and Samways

1998; Bomar 2001; Biedermann 2005), do not show the full picture of a habitat’s quality, and additional insect groups like hemipterans can further illuminate the story.

More recently, the composition of Auchenorrhyncha (leafhoppers and planthoppers) on restored heathlands in the UK has been shown to converge with that of remnant sites as time since restoration increases, indicating that hemipterans may be successfully restored, but it can take as much as 11 years (Mulio and Cherrill 2020). They also found that Auchenorrhyncha assemblage was similar between a created heathland and an adjacent mesotrophic grassland, indicating that hemipterans benefit from having close source sites (Mulio and Cherrill 2020). Habitat isolation from source habitats is a potential concern in restoration of the hemipteran community, as Rösch et al. (2013) found that more isolated habitats had lower leafhopper species richness than less isolated habitats. This phenomenon is further illustrated by a study conducted on restored and remnant prairies in a Kansas agricultural matrix, which found the same number of grassland specialist leafhoppers across all prairies (Keene et al. 2020). They ascribe this finding to an influx of migratory, generalist, agricultural pest species that were abundant at all sites. Thus, close proximity to agriculture, and conversely isolation from prairie sources is likely to affect the composition of hemipterans in the present study system as well.

It is also important to consider the size of habitat fragments, as many insect groups are known to have a close, positive relationship with habitat size (Krauss et al. 2003;

Meyer et al. 2007). Hemipterans, as well, have been shown to be affected by the size of their habitat (Biedermann 2002; Cronin 2003). The planthopper Prokelisia crocea was

3 found to increase in density and patch occupancy as the patch size of its host plant,

Spartina pectinata (prairie cordgrass) increased (Cronin 2003). Small patches also had fewer immigrants and more emigrants, putting them at greater risk of patch extinction

(Cronin 2003). Based on this background, I studied several variables that may influence hemipteran abundance and composition in restorations: status of prairie (i.e. constructed vs. remnant), age of construction, distance of prairie to agriculture (i.e. isolation from source habitat), and fragment size.

Here, I will focus on the Hemiptera and their response to restorations because they are abundant and diverse in grassland habitats (Nickel and Hildebrandt 2003;

Biedermann et al. 2005), can be easily sampled via sweepnet, and have been shown in several studies to reflect factors including time since restoration as well as management practices (Nickel and Hildebrandt 2003; Biedermann et al. 2005; Mulio and Cherrill

2020; Helden et al. 2020). To see if hemipterans can be used to evaluate prairie restorations in Ohio, I used a study system of 13 relatively small remnant and constructed prairies located in a matrix of agriculture and suburban areas. I determined whether the hemipteran community was restored within 7 constructed prairies compared to 6 native remnant prairies in the Miami Valley region, and used this information to answer 4 questions: Do older constructed prairies resemble remnant prairies in hemipteran abundance, diversity, and composition more than they resemble newer constructed prairies? Does the size of a prairie fragment affect the abundance, diversity, and composition of Hemiptera? Does the distance of a prairie to an agricultural field affect the abundance, diversity, and composition of Hemiptera? Do any hemipteran morphospecies indicate particular prairie types?

4 METHODS

Our lab took insect samples from 13 prairies in 4 southwestern Ohio counties

(Clark, Greene, Montgomery, and Miami). There were 6 remnant prairies (Broadwing,

Goode Prairie, Huffman, Prairie Grass Trail, Sandridge, and Stillwater), 4 old constructed prairies (Carriage Hill, Englewood, Possum Creek, and Sugar Creek), and 3 new constructed prairies (Leadingham, Medlar, Oaks Quarry) (Table 1). Remnant prairies are sites that are considered native, and have not been plowed or used for some other land use in photographic history; old constructed prairies are sites that have been reconstructed more than 20 years ago; and new constructed prairies are sites that have been reconstructed less than 20 years ago. A representative image of each prairie type is shown in Figure 1. Most of the prairies are located within a matrix of agriculture or suburban areas, and are all within 3 km of an agricultural field.

We collected insect samples in June, July, and August 2019 using sweepnets: each month, four sets of 25 sweeps were taken at each site. The insects collected at each prairie for each sampling day were stored in zip-lock bags and frozen at -18ºC. These samples were then sorted into insect orders during Fall 2019. I then removed hemipterans and further sorted them into family and morphospecies. To determine the effects of fragment size and distance to agriculture on hemipteran abundance and composition, I also measured the approximate size of each prairie and measured the distance to the closest agricultural field using Google Earth Pro version 7.3.3.7786. I measured size by tracing around each prairie and taking area in hectares, and I measured distance to

5 agriculture (km) by drawing a line from the edge of each prairie straight to the edge of the nearest agricultural field.

All data analysis was done in R version 3.6.2. To determine the effect of prairie type (remnant, old constructed, or new constructed) on several dependent variables (total hemipteran abundance, number of families, number of morphospecies, and Simpson’s

Diversity index), I first tested each dataset for normality and evenness using the Shapiro-

Wilk test and the Bartlett Test. I then performed a one-way ANOVA on datasets that were normally distributed, or the Kruskal-Wallis on datasets that were not normally distributed. If the result was significant, I then performed the Tukey HSD pairwise analysis or the non-parametric pairwise Wilcox test to determine pairwise significance between prairie types. I also ran this analysis on the abundance of common families

(more than 50 individuals within each month).

In order to determine the relationship between age of constructed prairie and hemipteran abundance and diversity, I ran four linear regressions using several different dependent variables (total hemipteran abundance, number of families, number of morphospecies, and Simpson’s Diversity index) with age of prairie as the independent variable. I also ran a correlation matrix on the abundance of all hemipteran families found in the entire dataset and within each month individually with age of prairie. I ran linear regressions on any common family (i.e. at least 10 individuals total that appeared in at least 3 sites) that had a significant correlation with age. Finally, for families that had either a significant difference in abundance between prairies types and/or a significant relationship with age of prairie, I determined the most dominant morphospecies (>5% of the family’s abundance within the given month), and analyzed the effect of prairie type

6 and age of constructed prairie on the abundance of each morphospecies as well, using the same methods as described above.

I used non-metric multi-dimensional scaling (NMDS) with the Bray-Curtis dissimilarity matrix to visualize the similarity in the composition of common morphospecies (>1% of the entire dataset) between prairie types for each month in summer 2019. To determine if prairie size or distance to agriculture affected hemipteran abundance or composition, I ran linear regressions using the dependent variables total

Hemiptera and number of families with prairie size and distance to agriculture as independent variables. I also ran correlation matrices using the dependent variables number of morphospecies, Simpson’s Diversity index, abundance of all families, and abundance of common morphospecies (>1% of the dataset). I ran linear regressions on any variables that showed a significant correlation with prairie size or distance to agriculture, as long as the family or morphospecies had at least 10 individuals and appeared in at least 3 prairies. To determine if there were any hemipteran morphospecies that indicated prairie type (remnant, old constructed, or new constructed prairies), I conducted an Indicator Species analysis on the full list of hemipteran families and on the common morphospecies (>1% of the dataset) for each month that Hemiptera were sampled.

7 RESULTS

From the 13 prairies sampled in summer 2019, I counted 5430 hemipterans from

31 families and 280 morphospecies. The most dominant family was Cicadellidae

(leafhoppers), making up 44.68% of all hemipterans found, followed by Miridae (plant bugs), which made up 14.11%, and Aphidoidea (aphids), which made up 13.24% (Table

2).

Overall, there was no difference in total hemipteran abundance, number of families, or number of morphospecies between the three prairie types in any month sampled (p>0.05 for all) (Fig. 2-4). There was also no significant relationship between age of constructed prairie and hemipteran abundance, number of families, number of morphospecies, or Simpson’s Diversity (p>0.05 for all) (Fig. 5-8). One hemipteran family, Psyllidae (jumping plant lice) had a significantly lower abundance in old constructed than in new constructed prairies in June 2019 (F2,10 =4.705, p=0.0363) (Fig.

9).

In June 2019, there were significant negative relationships between age of constructed prairie and both the number of Miridae (R2=0.6531, p=0.0278) and Psyllidae

(R2=0.8094, p=0.0058) (Fig. 10). These relationships were likely driven by the dominant morphospecies of each of these respective families: Lygus lineolaris (70% of all Miridae sampled in June 2019) had a significant negative relationship with age of construction in

June 2019 (R2=0.6557, p=0.0273) (Fig. 11). One morphospecies of the genus

Craspedolepta (known hereafter as Craspedolepta sp.) (97% of all Psyllidae sampled in

June 2019) also had a significant negative relationship with age of construction in June

2019 (R2=0.8094, p=0.0058) (Fig. 11). However, neither the abundance of L. lineolaris

8 or Craspedolepta sp. differed between the three prairie types in June 2019 (p>0.05 for both) (Fig. 12). Additionally, after removing one outlier remnant prairie, I found that remnant prairies had a significantly greater diversity (i.e., lower Simpson’s Index) in July

2019 than old constructed and new constructed prairies (F2,9=5.6933, p=0.0252) (Fig.

13). Using NMDS, I found that the composition of common morphospecies overlapped between the three prairie types in every month, except for August 2019 where composition of morphospecies in new constructed prairies diverged from that of both remnant and old constructed prairies (Fig. 14-16).

There was no significant relationship between total hemipteran abundance or number of hemipteran families and size of prairie or distance to agriculture (p>0.05 for all) (Tables 3 and 4). There was also no significant correlation for abundance of any of the common morphospecies, number of morphospecies, or Simpson’s index with size of prairie or distance to agriculture (p>0.05 for all variables). However, in July 2019, the family Membracidae (treehoppers) did have a significant positive relationship with distance of prairie to agriculture (R2=0.3398, p=0.0365) (Fig. 17). Finally, after performing an indicator species analysis, one morphospecies of Membracidae was identified as an indicator of remnant prairies in June 2019: Micrutalis calva (p=0.0430; indval=0.6875) (Table 5).

9 DISCUSSION

Overall findings

Here, hemipteran abundance and diversity generally did not differ between different prairie types, and was not affected by age of prairie construction (Fig. 1-7).

These results together suggest that, as a whole, the hemipteran community is not largely different between constructed prairies in this region and the native sites they seek to emulate. We did, however, find several interesting results which merit further study.

First, in June 2019, two morphospecies (Lygus lineolaris and Craspedolepta spp.) had a significant negative relationship with age of constructed prairie (Fig. 10). Second, in July

2019, hemipterans in remnant prairies had greater diversity than in either category of construction (Fig. 7). Third, in August 2019, the composition of morphospecies in new constructed prairies diverged from that of remnant and old constructed prairies (Fig. 13).

These findings suggest that while remnant and constructed prairies in this system are generally similar, the hemipteran community experiences seasonal differences between these prairie types.

Additionally, because size of prairie and distance to agriculture did not influence hemipteran composition, potentially all prairies in this system are of adequate size to support a similar community of Hemiptera, and they may all be close enough to agriculture for the effects to be similar across them. However, in July 2019, the family

Membracidae did significantly increase in prairies that were further away from agriculture (Fig. 14), which suggests that this family is negatively affected by close proximity to agriculture. In this section, I will discuss in more detail the aspects of the hemipteran community that were not affected by the variables in this study, and what this

10 means for our prairie restorations. I will also discuss the hemipteran groups that were affected, and what we can learn from these groups.

Question 1: Do older constructed prairies resemble remnant prairies in hemipteran abundance, diversity, and composition more than they resemble newer constructed prairies?

The hemipteran communities sampled in different prairies in this study as a whole appear largely the same between constructed and remnant prairies, which suggests that the constructed prairies adequately replicate the plant communities of native remnant prairies, which support similar groups of Hemiptera. There was also no significant relationship between either total hemipteran abundance, number of families, number of morphospecies, or Simpson’s Diversity and age of constructed prairie, which contrasts with findings from some other studies. For instance, Mulio and Cherrill (2020) found that leafhopper compositions in restored UK heathlands converged with that of remnant sites after about 11 years. This also contrasts with findings from this lab on these study sites, as Coleoptera communities in constructed prairies have previously been found to converge with those at remnant sites after about 30 years (Finke 2019). My finding here suggests that a minimum amount of time of around 6-7 years is sufficient to restore the hemipteran community to match remnant prairies.

Some studies that have looked at Hemiptera in restored prairies in agricultural networks also have not seen differences in hemipteran communities between restored and remnant prairies. For instance, Keene et al. (2020) performed a similar study and also found little difference in leafhopper diversity between remnant and reconstructed prairies.

11 Their study system also comprised of relatively small prairies distributed within a primarily agricultural system, which may have been a source for migratory insect pests.

A similar situation could be operating at our fields where all prairies are relatively near agriculture, and this may be confounding any effect of restoration itself. I identified one morphospecies as Lygus lineolaris (the Tarnished Plant Bug), a known crop pest in eastern North America (Tingey and Pillimer 1977; Young 1986).

Lygus lineolaris dominated the number of Miridae that were found in my insect samples, making up around 70% of all Miridae collected in June 2019. Although native to North America (Slater and Davis 1952), L. lineolaris is a widely known generalist insect pest which feeds on a vast variety of crops (Tingey and Pillimer 1977; Young

1986), including corn, soy beans, and fruit crops such as apples, all crops of economic value in Ohio (Neiswander 1931; Broersma and Luckmann 1970; Young 1986; Michaud et al. 1990). In addition, it is not limited to agriculture, also using native species such as goldenrod (Cleveland 1982). Being a versatile generalist, it makes sense that this species dominates the Miridae in our constructed prairies, which are all within 3 km of agriculture. It is also possible that L. lineolaris is outcompeting other mirids for resources and homogenizing the Hemiptera in this network of prairies.

A second hemipteran morphospecies was also found to have a significant negative relationship with age of constructed prairie: Craspedolepta spp. Although this morphospecies was not identified to species, it also dominated its respective family, the

Psyllidae or jumping plant lice, making up 97% of psyllids collected in June 2019. This morphospecies also declined in constructed prairies as age increased in June 2019. Most species of psyllid are host specialists (Hodkinson 2009), and many species of

12 Craspedolepta feed on prairie perennials like Asteraceae (Hodkinson and White 1979). It is likely that these native perennials are present in the initial seed mixes when constructed prairies are started, but slowly disappear over time if the prairies are maintained with excessive mowing. Hemiptera are known to respond negatively to intense land management (Biedermann 2005), so this could represent an impediment to other prairie specialist Hemiptera in the area.

Finally, NMDS results showed that the composition of morphospecies of new constructed prairies diverged from that of remnant and old constructed prairies in August

2019 only, suggesting that while the prairie constructions may be on the right track in the early season, more time is needed for them to fully converge with remnant sites, as shown in other studies (Finke 2019; Mulio and Cherrill 2020). Midwestern tallgrass prairies grow and flower between June, July, and August, but peak in biomass more toward August (Briggs and Knapp 1995; Craine et al. 2012). Perhaps by the time the plant community is fully developed in the season, the disparities between the newer constructed prairies become more apparent, causing them to diverge. While the three prairies types are effectively similar during the early summer, they diverge during the peak growing season, indicating that the restoration of the Hemiptera community may not be complete at these restoration sites, or that other factors are affecting them. This idea is also supported by the fact that hemipteran diversity was significantly higher in remnant prairies in July 2019 than in old constructed and new constructed prairies (Fig. 12).

13 Question 2: Does the size of a prairie fragment affect the abundance, diversity, and composition of Hemiptera?

While others have found habitat size to be important to hemipteran abundance and composition (Biedermann 2002; Cronin 2003), I found no significant correlation between size of prairie fragment and total Hemiptera, number of families or morphospecies, abundance of any individual families or morphospecies, or Simpson’s Diversity. These data suggest that fragment size is not inherently important to Hemiptera, which sets them apart from other groups of insects like pollinators. For example, bees, butterflies, beetles, and flies have been shown to increase in abundance and richness as fragment size increases (Krauss et al. 2003; Meyer et al. 2007). Since individual species of Hemiptera often utilize one plant source throughout their life history, they may not have habitat needs as complex as other insects, and thus do not need as much space (Nickel 2003;

Rösch et al. 2013). Therefore, the range of prairie sizes used in our study may be sufficient to support an adequate population of Hemiptera.

In a study by Rösch et al. (2013), which used a grassland system to investigate how factors like fragment size, connectivity, and landscape complexity affected the distribution of leafhoppers, prairie fragments between 0.1 and 0.6ha were considered small, while fragments between 1.2 and 8.8ha were considered large. The sizes of prairies in the present study ranged from 0.45ha-46.5ha, with the majority being below 10ha, and only 2 above 20ha. Rösch et al. (2013) also found no direct relationship between leafhopper abundance or diversity with fragment size, which suggests that the range of sizes used in the present study are well above what might be needed to see a difference in hemipteran composition.

14 However Rösch et al. (2013) did find that the richness of generalist leafhopper species increased in small fragments as they became less isolated (Rösch et al. 2013).

Similarly, Batáry et al. (2021), who used the same grassland system as Rösch et al.

(2013), found that specialist leafhoppers were more abundant in large and well-connected prairie fragments, while small but well-connected habitats had more generalists.

Therefore, because specialist and generalist Hemiptera have contrasting responses to prairie size and connectivity, this could make the overall trend less clear for the

Hemiptera community as a whole.

Question 3: Does the distance of a prairie to an agricultural field affect the abundance, diversity, and composition of Hemiptera?

I found that the distance of individual prairies from the nearest agricultural field had no significant relationship with total Hemiptera, number of families, number of morphospecies, abundance of any morphospecies, or Simpson’s Diversity. All prairies in this system but one were within 1km of the nearest agricultural field, which is an easily traversable distance for winged insects (Stein 1986). Considering most of the prairies in our study system are located within a matrix of agriculture, and thus isolated from native prairie source habitats, this also supports findings by Rösch et al. (2013) that increased habitat isolation leads to decreased species richness in leafhoppers; if they are all effectively equally isolated, then a clear connection between distance to agriculture and the hemipteran community cannot be drawn. I also identified one pest species of Miridae,

Lygus lineolaris, which dominated the Miridae that were collected. It is possible that this species travels back and forth between agriculture and prairie, given its eclectic diet

15 (Tingey and Pillimer 1977; Cleveland 1982; Young 1986). This generalist pest may be one among many that can easily travel the short distances between most prairies in this system and the agricultural fields surrounding them, negating any difference that might be seen between prairies.

There was also one hemipteran family, Membracidae, that increased in abundance in prairies that were further from agriculture in July 2019 (Figure 14), which suggests that proximity to agriculture has a negative effect on this family. The Membracidae, or treehoppers, are uniquely shaped Hemiptera, often with elaborate pronotums. They are a diverse family that mainly feeds on trees, but many species also feed on herbaceous plants (Kopp and Yonke 1973; Wood 1993). While there are some polyphagous species, many in the north temperate region are host specific (Funkhouser 1917; Wood and

Olmstead 1984; Wood 1984; Wood 1993). It is possible that close proximity to agriculture exposes prairies to chemical runoff, which limits plant species diversity. This phenomenon would in turn limit the variety of hosts available for Membracidae, and lead to their decline in prairies that are closer to agriculture.

Question 4: Do any hemipteran morphospecies indicate particular prairie types?

This study found one morphospecies of Membracidae, Micrutalis calva (honey locust treehopper) that was an indicator of remnant prairies in June 2019 (Table 6). This species of treehopper is known to be polyphagous, feeding on both woody species such as Gleditsia treiacanthos (honey locus) and Quercus palustris (pin oak), as well as herbaceous species such as Ambrosia sp. (ragweed), Helianthus sp. (sunflower), and

Vernonia noveboracensis (ironweed) (Kopp and Yonke 1973; Nixon and Thompson

16 1987; Johnson and Freytag 1997). Despite being polyphagous, this species relies on several prairie species, which may not be present at constructed prairies. In July 2019, the family Membracidae also declined with increased proximity to agriculture (Fig. 14), which suggests that members of this family have difficulty crossing agricultural fields to travel between prairies. Thus, even if suitable host plants are present at constructed prairies, M. calva might not be able to colonize them efficiently.

Overall conclusion

While the findings of this study indicate few differences in Hemiptera composition between broad factors such as prairie type, age, size, and distance to agriculture, this does not mean that hemipterans should not be used in prairie restoration evaluations. In fact, the differences that were found within specific groups between prairie types throughout the summer suggest that more in-depth studies should be done on this insect group. Both Lygus lineolaris and Craspedolepta spp. were shown to have a significant negative relationship with age of constructed prairie in early summer. It could be informative to sample insects in surrounding agricultural fields to see if L. lineolaris is utilizing agricultural fields as well. More in-depth data on the plant community of prairie constructions can also serve to explain the decline of Cradepolepta sp. This could mean that more work needs to be done to maintain prairie restorations long term.

The family Membracidae was found to increase in abundance in prairies that were further from agriculture, suggesting that this family is negatively affected by proximity to agriculture. In addition, Micrutalis calva was found to be an indicator of remnant prairies in June 2019; since M. calva and other membracids are mainly tree and herbaceous

17 prairie plant feeders (Funkhouser 1917; Kopp and Yonke 1973; Wood 1993), it is possible that they struggle to cross agricultural fields. This group should be investigated in more depth, to learn how the agricultural matrix in this region is affecting the potential of Ohio prairie restoration. In addition, surveys of plant composition in all prairies can be used to potentially explain the relationship that membracids have with our prairies, as well as the differences seen in the hemipteran community in July and August. Finally, data could be taken on the connectivity of these prairies to each other and to other source habitats, to learn more about how hemipterans are moving across this system.

The results of this current study confirm that the Hemiptera are a promising insect group to use in prairie restoration research. The Miridae, Psyllidae, and Membracidae are three families that have shown interesting relationships with the various traits of the remnant and constructed prairies in this system, and can inform us about areas where the maintenance of prairie constructions in this region could be improved. The changes in the

Hemiptera community that I observed across 3 months in summer 2019 indicate that the

Hemiptera can reflect seasonal changes in prairie restorations, and help us continue to evaluate these efforts in the future.

18 FIGURES

Figure 1: Representative images of the three prairie types used in this study. (A) Remnant prairie- Huffman. (B) Old constructed prairie- Possum Creek. (C) New constructed prairie- Leadingham.

June 2019

A 0

t p

l a

t o

T 0

Remnant Old Constructed New Constructed Prairie Type

July 2019

0 5

B 3 0

a 5

0 e

o 0

5 1

0 0

1 0 5 Remnant Old Constructed New Constructed Prairie Type August 2019

0 0

C 5 0

r e

T 0

0 2

0 0 1

Remnant Old Constructed New Constructed

Prairie Type

Figure 2: Box and whisker plots showing the total Hemiptera sampled at each prairie type in each month of summer 2019. (A) June [Kruskal-Wallis chi-squared=3.7253, df=2, p=0.1553]. (B) July [Kruskal-Wallis chi-squared=0.8132, df=2, p=0.6659]. (C) August [Kruskal-Wallis chi-squared=0.47253, df=2, p=0.7896].

20 June 2019

A 1 1

e i

e b

u 8 N

Remnant Old Constructed New Constructed Prairie Type

July 2019

B 4

2 1

m a

r e

u N

Remnant Old Constructed New Constructed

Prairie Type

August 2019

C 4 1

l i

m u

6 Remnant Old Constructed New Constructed Prairie Type Figure 3: Box and whisker plots showing the number of hemipteran families sampled at each prairie type in each month of summer 2019. (A) June [Kruskal-Wallis chi- squared=5.2514, df=2, p=0.0724]. (B) July [Kruskal-Wallis chi-squared=0.54391, df=2, p=0.7619]. (C) August [Kruskal-Wallis chi-squared=1.8655, df=2, p=0.3955].

21 June 2019

A 0

c e

o h

r e

N 5

Remnant Old Constructed New Constructed Prairie Type

July 2019

0 B 5

c e

h p

e b

0 N 2

Remnant Old Constructed New Constructed Prairie Type

August 2019

C 0

5 5

c e

h p

b 3

N 5

0 2

New Constructed Old Constructed Remnant

Prairie Type

Figure 4: Box and whisker plots showing the number of hemipteran morphospecies sampled at each prairie type in each month of summer 2019. (A) June [Kruskal-Wallis chi-squared=1.2687, df=2, p=0.5303]. (B) July [Kruskal-Wallis chi-squared=0.0470, df=2, p=0.9768]. (C) August [Kruskal-Wallis chi-squared=1.8595, df=2, p=0.3947].

22 A B C

June 2019 July 2019 August 2019

0 5

10 15 20 25 30 35 40 10 15 20 25 30 35 40 10 15 20 25 30 35 40 Age of constructed prairie Age of constructed prairie Age of constructed prairie

Figure 5: Linear models showing the relationship between total Hemiptera and age of constructed prairie in each month of summer 2019. (A) June [R2=0.182, p=0.3399]. (B) July [R2=0.0882, p=0.5179]. (C) August [R2= 0.0940, p=0.5036].

23 A B C

June 2019 July 2019 August 2019

6 6

10 15 20 25 30 35 40 10 15 20 25 30 35 40 10 15 20 25 30 35 40 Age of constructed prairie Age of constructed prairie Age of constructed prairie

Figure 6: Linear models showing the relationship between number of hemipteran families and age of constructed prairie in each month of summer 2019. (A) June [R2=0.2807, p=0.2213]. (B) July [R2=0.1462, p=0.3972]. (C) August [R2= 0.0145, p=0.7968].

24 A B C

June 2019 July 2019 August 2019

0 2

10 15 20 25 30 35 40 10 15 20 25 30 35 40 10 15 20 25 30 35 40 Age of constructed prairie Age of constructed prairie Age of constructed prairie

Figure 7: Linear models showing the relationship between number of hemipteran morphospecies and age of constructed prairie in each month of summer 2019. (A) June [R2=0.2346, p=0.2707]. (B) July [R2=0.0406, p=0.6649]. (C) August [R2= 0.0071, p=0.8571].

25 A B C

June 2019 July 2019 August 2019

. 0

10 15 20 25 30 35 40 10 15 20 25 30 35 40 10 15 20 25 30 35 40 Age of constructed prairie Age of constructed prairie Age of constructed prairie

Figure 8: Linear models showing the relationship between Simpson’s Diversity Index and age of constructed prairie in each month of summer 2019. (A) June [R2=0.0192, p=0.7673]. (B) July [R2=0.0420, p=0.6593]. (C) August [R2= 0.0304, p=0.7083].

Psyllidae

2 AB B e

d i

l 2

y s

f 1

0 b

u N 5 A

0 Remnant Old Constructed New Constructed Prairie Type Figure 9: Box and whisker plots showing the abundance of Psyllidae (jumping plant lice) across the 3 prairie types in June 2019. Psyllidae had significantly greater abundance in new constructed than old constructed prairies (ANOVA (F2,10 =4.705, p=0.0363)

Miridae Psyllidae

0 0

10 15 20 25 30 35 40 10 15 20 25 30 35 40 Age of constructed prairie Age of constructed prairie

Figure 10: Linear model showing the relationship between the abundance of 2 hemipteran families and age of constructed prairie in June 2019. Miridae (plant bugs) had a significant negative relationship with age of prairie (R2=0.6531, p=0.0278), and Psyllidae had a significant negative relationship with age of prairie (R2=0.8094, p=0.0058).

Lygus lineolaris Craspedolepta sp.

0 0

10 15 20 25 30 35 40 10 15 20 25 30 35 40 Age of constructed prairie Age of constructed prairie

Figure 11: Linear model showing the relationship between the abundance of 2 hemipteran morphospecies and age of constructed prairie in June 2019. One morphospecies of Miridae, Lygus lineolaris, had a significant negative relationship with age of constructed prairie (R2=0.6557, p=0.0273). One morphospecies of Psyllidae, Craspedolepta sp., had a significant negative relationship with age of constructed prairie in June 2019 (R2=0.8094, p=0.0058).

Lygus lineolaris Craspedolepta sp.

i s

l t

o p

e e

r o

0 0

Remnant New Constructed Remnant New Constructed Prairie Type Prairie Type

Figure 12: Box and whisker plots showing the difference in abundance of 2 hemipteran morphospecies between the 3 prairie types in June 2019. Neither morphospecies had a significantly different abundance. Lygus lineolaris [Kruskal-Wallis chi-squared=2.967, df=2, p=0.2269]. Crapedolepta sp. [Kruskal-Wallis chi-squared=5.6667, df=2, p=0.0588].

Simpson's Diversity July 2019

. 0

B B

s .

' A

. 0 Remnant Old Constructed New Constructed Prairie Type

Figure 13: Box and whisker plot showing the difference in Simpson’s Diversity Index between the three prairie types in July 2019. Simpson’s Diversity Index was lower in remnant prairies than at old constructed and new constructed prairies (ANOVA F2,9=5.6933, p=0.0252). Lower Simpson’s Diversity Index indicates greater diversity.

Figure 14: NMDS showing the composition of 21 abundant hemipteran morphospecies (those that make up >1% of the entire dataset) in June 2019 (k=2; stress=0.1194). The composition of all three prairie types overlaps.

Figure 15: NMDS showing the composition of 21 abundant hemipteran morphospecies (those that make up >1% of the entire dataset) in July 2019 (k=2; stress=0.1886). The composition of all three prairie types overlaps.

Figure 16: NMDS showing the composition of 21 abundant hemipteran morphospecies (those that make up >1% of the entire dataset) in August 2019 (k=2; stress=0.1591). The composition new constructed prairies diverges from remnant and old constructed prairies in this month.

Membracidae

1 0

0.0 0.5 1.0 1.5 2.0

Distance to agriculture (km)

Figure 17: Linear model showing the relationship between the abundance of Membracidae and distance to agriculture July 2019. Membracidae abundance increased significantly as distance to agriculture increased (R2=0.3398, p=0.0365).

35 TABLES

Table 1: Information about all prairies sampled in this study. Age in Distance to Prairie Name Prairie Type 2019 Size (ha) Agr. (km) Coordinates Sampling Period June, July, Broadwing Remnant n/a 0.45 0.41 39.643028, -84.413313 August 2019 June, July, Goode Prairie Remnant n/a 2.94 0.01 40.167111, -84.404563 August 2019 June, July, Huffman Remnant n/a 46.5 2.23 39.807224, -84.059347 August 2019 June, July, Prairie Grass Trail Remnant n/a 0.25 0.04 39.7888, -83.7130 August 2019 June, July, Sandridge Remnant n/a 1.3 0.5 39.716369, -84.210578 August 2019 June, July, Stillwater Remnant n/a 0.5 0.17 40.1542056, -84.384502 August 2019 June, July, Carriage Hill Old Constructed 23 5.69 0.03 39.879942, -84.094800 August 2019 June, July, Englewood Old Constructed 26 7.24 0.34 39.867591, -84.269053 August 2019 June, July, Possum Creek Old Constructed 39 23.6 0.23 39.7139806, -84.266438 August 2019 June, July, Sugar Creek Old Constructed 34 9.1 0.07 39.617715, -84.092614 August 2019 June, July, Leadingham New Constructed 7 4.12 0.01 39.877786, -83.999432 August 2019 June, July, Medlar New Constructed 7 16.2 0.03 39.603960, -84.258753 August 2019 June, July, Oaks Quarry New Constructed 16 0.45 0.59 39.8160472, -83.99199 August 2019

36 Table 2: Total specimens collected of each hemipteran family in summer 2019.

Family Total summer 2019 Acanaloniidae 61 Aleyrodidae 139 Anthocoridae 87 Aphidoidea 719 Berytidae 4 Blissidae 42 Caliscelidae 3 Cercopidae 125 Cicadellidae 2426 Cixiidae 29 Coreidae 6 Cydnidae 9 Cymidae 19 Delphacidae 308 Derbidae 3 Dictyopharidae 26 Flatidae 1 Lygaeoidea 3 Membracidae 142 Miridae 766 Nabidae 19 Pachygronthidae 193 Pentatomidae 56 Phymatidae 6 Piesmatidae 1 Psyllidae 150 Reduviidae 13 Rhopalidae 3 Rhyparochromidae 4 Thyreocoridae 14 Tingidae 21 Unknown Heteropteran 11 Unknown Homopteran 3 Unknown 18

37 Table 3: Table showing results of linear regressions on the relationship between size of prairie and total Hemiptera and number of families. None have a significant relationship.

June, 2019 2 Parameter R p-value Total Hemiptera 0.021 0.6405 Number of families 0.05579 0.4372

July, 2019 Parameter R2 p-value Total Hemiptera 0.0497 0.4643

Number of families 0.0875 0.3264

August, 2019

2 Parameter R p-value Total Hemiptera 0.0387 0.5197 Number of families 0.0635 0.4061

38 Table 4: Table showing results of linear regressions on the relationship between distance of prairie to agriculture and total Hemiptera and number of families. None have a significant relationship.

June, 2019 Parameter R2 p-value Total Hemiptera 0.1942 0.3957 Number of families 0.0510 0.4580

July, 2019 Parameter R2 p-value

Total Hemiptera 0.0966 0.3013 Number of families 0.0004 0.9454

August, 2019

Parameter R2 p-value Total Hemiptera 0.0556 0.4380 Number of families 0.0009 0.9236

Table 5: Table showing indicator analysis output for Micrutalis calva in June 2019.

Relative abundance Indicator value p- Morphospecies indval R OC NC R OC NC value Micrutalis 0.0430 0.6875 0.6875 0.2500 0.0625 0.6875 0.1875 0.0410 calva

40 REFERENCES

Batáry, P., V. Rösch, C. F. Dormann, and T. Tscharntke. 2021. Increasing connectivity enhances habitat specialists but simplifies plant-insect food webs. Oecologia 195:539-546.

Biedermann, R. 2002. Leafhoppers (Homoptera, Auchenorrhyncha) in fragmented habitats. Denisia 4: 523-530.

Biedermann, R. R. Achtziger, H. Nickel, and A.J.A. Stewart. 2005. Conservation of grassland leafhoppers: a brief review. Journal of Insect Conservation 9: 229-43.

Bomar, C. R. 2001. Comparison of grasshopper (Orthoptera: Acrididae) communities on remnant and reconstructed prairies in western Wisconsin. Journal of Orthoptera Research 10:105-112.

Briggs, J. M., and A. K. Knapp. 1995. Interannual variability in primary production in tallgrass prairie: climate, soil moisture, topographic position, and fire as determinants of aboveground biomass. American Journal of Botany 82:1024- 1030.

Broersma, D. B., and W. H. Luckmann. 1970. Effects of Tarnished Plant Bug feeding on soybean. Journal of Economic Entomology 63:253-256.

Chambers, B. Q., and M. J. Samways. 1998. Grasshopper response to a 40-year experimental burning and mowing regime, with recommendations for invertebrate conservation management. Biodiversity and Conservation 7:985-1012.

Cleveland, T. C. 1982. Hibernation and host plant sequence studies of Tarnished Plant Bugs, Lygus lineolaris, in the Mississippi Delta. Environmental Entomology 11:1049-1052.

Craine, J. M., E. M. Wolkovich, E. G. Towne, and S. W. Kembel. 2012. Flowering phenology as a functional trait in a tallgrass prairie. New Phytologist 193:673- 682.

Cronin, J. T. 2003. Movement and spatial population structure of a prairie planthopper. Ecology 84:1179-1188.

Dobson, A. P., A. D. Bradshaw, and A. Baker. 1997. Hopes for the future: restoration ecology and conservation biology. Science 277:515-522.

Ehrlich, P. R. 1961. Intrinsic barriers to dispersal in Checkerspot Butterfly. Science 134:108-109.

Finke, A. N. 2019. If we build it, will they come? Insect communities as indicators of restoration in an urban prairie network (Master’s Thesis, University of Dayton).

Five Rivers Metroparks. Conservation Leadership: How We Do It. 2021. Web. 2/20/21

Funkhouser, W. D. 1917. Biology of the Membracidae of the Cayuga Lake Basin (PhD Thesis, Cornell University).

Helden, A. J., J. Chipps, S. McCormack, and L. Pereira. 2020. Is grazing always the answer to grassland management for arthropod biodiversity? Lessons from a gravel pit restoration project. Journal of Insect Conservation 24:655-670.

Hodkinson, I.D. and White, I.M. 1979. Handbooks for the identification of British insects: Homoptera: Psylloidea Volume II, Part 5(a). Royal Entomological Society, London, UK.

Hodkinson, I.D. 2009. Life cycle variation and adaptation in jumping plant lice (Insecta: Hemiptera: Psylloidea): a global synthesis. Journal of Natural History 43:65-179.

Holl, K. D. 1995. Nectar resources and their influence on butterfly communities on reclaimed coal surface mines. Restoration Ecology 3:76-85.

Johnson, M. P., and P. H. Freytag. 1997. Treehoppers (Homoptera: Membracidae) on pin oak in Kentucky. Journal of the Kansas Entomological Society 70:21-30.

Keene, K., C. M. Malmstrom, H. M. Alexander, A. Wayadande, and K. R. Denning. 2020. Low conservatism of leafhopper communities in remnant and reconstructed prairie sites in a working agroecological landscape. Journal of Insect Conservation 24:35-48.

Kopp, D. D. and T. R. Yonke. 1973. The Treehoppers of Missouri: Part 2. Subfamily Smiliinae; Tribes Acutalini, Ceresini, and Polyglyptini (Homoptera: Membracidae). Journal of the Kansas Entomological Society 46:233-276.

Klopatek, J. M., R. J. Olson, C. J. Emerson, and J. L. Joness. 1979. Land-use conflicts with natural vegetation in the United-States. Environmental Conservation 6:191-199.

Knopf, F. L. 1986. Changing landscapes and the cosmopolitism of the eastern Colorado avifauna. Wildlife Society Bulletin 14:132-142.

42 Krauss, J., I. Steffan-Dewenter, and T. Tscharntke. 2003. How does landscape context contribute to effects of habitat fragmentation on diversity and population density of butterflies? Journal of Biogeography 30:889-900.

Longcore, T. 2003. Terrestrial arthropods as indicators of ecological restoration success in coastal sage scrub (California, USA). Restoration Ecology 11:397-409.

Meyer, B., V. Gaebele, and I. D. Steffan-Dewenter. 2007. Patch size and landscape effects on pollinators and seed set of the horseshoe vetch, Hippocrepis comosa, in an agricultural landscape of central Europe. Entomologia Generalis 30:173-185.

Michaud, O. D., R. K. Steward, and G. Boivin. 1990. Susceptibility of Apples to Damage by Lygocoris communis and Lygus lineolaris (Hemiptera: Miridae). Phytoprotection 71:25-30.

Millennium Ecosystem Assessment 2005. Ecosystems and Human Well-Being: Biodiversity Synthesis (available from https://www.millenniumassessment.org/en/Synthesis.html) accessed in December 2019. World Resources Institute, Washington, D.C.

Mulio, S. A., and A. Cherrill. 2020. Re-establishment of Auchenorrhyncha (Hemiptera) assemblages following heath and grassland habitat creation on lowland farmland. Annales Zoologici Fennici 57:1-10.

Neiswander, C.R. 1931. The sources of American corn insects. Ohio Agricultural Experiment Station. Bulletin 473: 1-98.

Nemec, K. T., and T. B. Bragg. 2008. Plant-feeding Hemiptera and Orthoptera communities in native and restored mesic tallgrass prairies. Restoration Ecology 16:324-335.

Nickel, H. 2003. The leafhoppers and planthoppers of Germany (Hemiptera, Auchenorryncha): Patterns and Strategies in a Highly Diverse Group of Phyotophagous Insects. PENSOFT, Sofia, Bulgaria.

Nickel, H., and J. Hildebrandt. 2003. Auchenorrhyncha communities as indicators of disturbance in grasslands (Insecta, Hemiptera) - a case study from the Elbe flood plains (northern Germany). Agriculture Ecosystems & Environment 98:183-199.

Nixon, P. L., and H. E. Thompson. 1987. Biology of Micrutalis calva (Homoptera,Membracidae) on honey locust. Journal of the Kansas Entomological Society 60:273-279.

Panzer, R. 1988. Managing Prairie Remnants for Insect Conservation. Natural Areas Journal 8:83-90.

43 Rösch, V., T. Tscharntke, C. Scherber, and P. Batáry. 2013. Landscape composition, connectivity and fragment size drive effects of grassland fragmentation on insect communities. Journal of Applied Ecology 50:387-394. Ruiz-Jaen, M. C., and T. M. Aide. 2005. Restoration Success: How is it being measured? Restoration Ecology 13: 569-77.

Samson, F., and F. Knopf. 1994. Prairie conservation in North-America. Bioscience 44: 418-21.

Slater, J.A. N.T. Davis. 1952. The scientific name of the Tarnished Plant Bug. Proceedings of the Entomological Society of Washington 54: 194-198.

Stein, W. 1986. Dispersal of Insects of Public Health Importance. Pages 242- 252 In Danthanarayana, editor. Insect Flight, Springer-Verlag, Berlin, Germany.

Suding, K. N., K. L. Gross, and G. R. Houseman. 2004. Alternative states and positive feedbacks in restoration ecology. Trends in Ecology & Evolution 19:46-53.

Tian, G., L. Brussaard, B.T. Kang, and M.J. Swifty. 1997. Soil fauna-mediated decomposition of plant residues under constrained environment and residue quality conditions. Pages 125-134 In Cadisch, G., and K. E. Giller, editors. Driven by Nature: Plant Litter Quality and Decomposition, CAB International, Wallingford, Oxon.

Tingey, W.M. and Pillimer, E.A. 1977. Lygus Bugs: Crop resistance and physiological nature of feeding injury. Bulletin of Entomological Society of America 23:277- 287.

Transeau, E. N. 1935. The Prairie Peninsula. Ecology 16:423-437.

Wood, T. K. 1993. Diversity in the New World Membracidae. Annual Review of Entomology 38:409-435.

Wood, T. K. 1984. Life history patterns of tropical Membracids (Homoptera: Membracidae). Sociobiology 8:299-344.

Wood, T. K., and K. L. Olmstead. 1984. Latitudinal effects on treehopper species richness (Homoptera, Membracidae). Ecological Entomology 9:109-115.

Young, O. P. 1986. Host plants of the Tarnished Plant Bug, Lygus lineolaris (Heteroptera: Miridae). Annals of the Entomological Society of America 79:747- 762.