University of Florida Thesis Or Dissertation Formatting

EVALUATING SOIL MITIGATION TACTICS AND ALTERNATE SHRUB SELECTION TO CREATE MORE SUSTAINABLE RESIDENTIAL LANDSCAPES

MATTHEW AMOS BORDEN

A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE

UNIVERSITY OF FLORIDA

2020

To my parents, Jeffrey and Patricia, and Grandmother CJ

ACKNOWLEDGMENTS

First, I wish to thank my parents for fostering an environment of learning and curiosity about the natural world from a young age, and for supporting my career path at each step. I also thank Grandmother CJ and late Grandfather Noel Borden for their many years of encouragement and generous financial support given towards my undergraduate education.

Next, I wish to express deep appreciation Dr. Adam Dale, my major advisor. I have often said there is no other lab I would rather have landed in here, and I remain immensely grateful.

Adam has been a role model of perseverance with good attitude, excellence in writing skills, and ambition in the pursuit of rigorous experiments and data that can make a difference in improving our environment. I am also grateful that he afforded me many opportunities for extension writing, speaking engagements, conference attendance, for supporting my interest in tea plants and associated pests, and for tolerating my many side-projects and scattered plant collections.

I also thank the members of the Dale Lab for their support, baked goods, and friendship; particularly Dr. Nicole Benda, who coordinated much of the field work, thatch analysis, and EPN experiment. I am extremely grateful to all those who endured hot Florida days or counting thousands of organisms to assist with data collection and plant care, including Lauren Dana,

Mark Wilhelm, Alex LoCastro, Kendall Stacey, Tanner Felbinger, and Rebecca Perry.

Lastly, I thank several other advisors: Dr. Amanda Hodges, who made it possible to study concurrently in the DPM program and provided many professional development opportunities; committee members Dr. Adam Dale and Dr. Oscar Liburd for reviewing this thesis; Dr. Keith

Yoder, who supported my pursuit of graduate education from afar; Lyle Buss, who provided photography resources and many pleasant insect mystery conversations; and Dr. Jay Stipes, who offered great wisdom, friendship, and the gift of his personal library.

TABLE OF CONTENTS

page

ACKNOWLEDGMENTS ...... 4

LIST OF TABLES ...... 7

LIST OF FIGURES ...... 8

ABSTRACT ...... 9

CHAPTER

1 LITERATURE REVIEW ...... 10

Challenges Associated with Urban Landscapes ...... 10 System I – Soil Mitigation for Lawns ...... 11 Benefits and Challenges Associated with Urban Landscapes ...... 11 Soil Mitigation Strategies ...... 12 System II – Shrub Selection ...... 13 Tea Scale: an Armored Scale Insect Pest ...... 14 Tea Scale Management ...... 16 Camellia sinensis: Potential in the Landscape ...... 18 Ilex vomitoria: Potential in the Landscape ...... 19 Summary of Other Plant-Ecosystem Interactions ...... 21 Research Objectives and Thesis Structure ...... 24

2 EFFECTS OF SOIL MITIGATION PRACTICES ON TERRESTRIAL INVERTEBRATES FOLLOWING RESIDENTIAL DEVELOPMENT ...... 25

Abstract ...... 25 Introduction ...... 26 Materials and Methods ...... 29 Study Site ...... 29 Experimental Design ...... 30 Survey of Lawn-dwelling Invertebrates ...... 31 Quantifying Detritivores and Thatch Decomposition ...... 32 Entomopathogenic Nematode Biological Control ...... 33 Statistical Analysis ...... 34 Results...... 35 Survey of Lawn-dwelling Invertebrates ...... 35 Detritivores and Thatch Decomposition ...... 36 Entomopathogenic Nematode Biological Control ...... 36 Discussion ...... 37 Acknowledgements ...... 40

3 NATIVE AND EDIBLE PLANTS ENHANCE ECOSYSTEM SERVICES THROUGH KEY PEST AVOIDANCE AND MULTIFUNCTIONALITY IN RESIDENTIAL LANDSCAPES...... 52

Abstract ...... 52 Introduction ...... 53 Materials and Methods ...... 57 Study Organisms ...... 57 Tea Scale Inoculations ...... 57 Host Susceptibility Evaluation ...... 58 Statistical Analysis ...... 59 Results...... 60 Host Susceptibility ...... 60 Host Plant Damage ...... 61 Discussion ...... 62 Acknowledgements ...... 67

4 CONCLUSIONS ...... 71

LIST OF REFERENCES ...... 73

BIOGRAPHICAL SKETCH ...... 86

LIST OF TABLES

Table page

2-1 Results of ANOVA models to examine the effects of treatment, sampling date, the interaction of treatment and date...... 51

3-1 Susceptibility of Ilex and Camellia species to Fiorinia theae, as measured by the number of infested leaves per plant, total and gravid females per infested leaf, and the susceptibility metric ...... 68

3-2 Mottling damage observed on Ilex and Camellia species due to Fiorinia theae feeding, as measured by the number of infested leaves per plant, percentage of infested leaves with mottling, and their product as a damage metric ...... 69

3-3 Number of leaves and percentage of leaves infested with Fiorinia theae, that prematurely abscised from Ilex spp. during an environmentally stressful period in late summer...... 70

LIST OF FIGURES

Figure page

2-1 Aerial view of study site showing the nine properties (lot 3-5, 7, 12-16), three outlined blocks, and three treatments within each block ...... 41

2-2 Lot during development, demonstrating typical site disturbance and soil compaction prior to plant installation...... 42

2-3 Example of backyard lawns at our study site, where each treatment was incorporated into the soil before plant installation on each lot...... 43

2-4 Overall arthropod abundance over the 2017-2018 survey period...... 44

2-5 Overall arthropod richness at order level over the 2017-2018 survey period ...... 45

2-6 Combined decomposer abundance over the 2017-2018 survey period...... 46

2-7 Increasing levels of thatch decomposition as measured by mean % carbon lost through LOI analysis (±SEM)...... 47

2-8 Waxworm infection rate after exposure to soil samples for 9 days (mean ±SEM), collecting at three dates in the 2017 and 2018 seasons ...... 48

2-9 Hunting billbug (Sphenophorus venatus vestitus) abundance over the 2017-2018 survey, collected by pitfall trapping (mean ±SEM) ...... 49

2-10 Combined natural enemy abundance over the 2017-2018 survey, collected by pitfall trapping (mean ±SEM) ...... 50

3-1 Host susceptibility metric (mean  SEM) of Ilex and Camellia spp. shrubs to tea scale, Fiorinia theae. The susceptibility metric is the product of the number of infested leaves per plant and number of gravid females per infested leaf ...... 68

3-2 Mottling damage metric (mean  SEM) of Ilex and Camellia spp. shrubs infested with tea scale, Fiorinia theae. Damage is the product of the number of infested leaves per plant and mean percent of leaves with visible mottling...... 69

3-3 Inoculation method demonstrating the pinned leaf used to inoculate new host plants ...... 70

Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science

EVALUATING SOIL MITIGATION TACTICS AND ALTERNATE SHRUB SELECTION TO CREATE MORE SUSTAINABLE RESIDENTIAL LANDSCAPES

Matthew A. Borden

May 2020

Chair: Adam G. Dale Major: Entomology and Nematology

The effects of rapid urbanization on humanity and our environment are becoming more far-reaching. Unfortunately, these landscapes face widespread problems of disturbed soil and environmental conditions that cause plant stress, reducing their functionality and increasing the need for maintenance inputs. Further, the ecosystem service contributions of plants selected to fill these landscapes may be inadequately evaluated, losing potential to maximize benefits such as pest resistance and reduced insecticide use. We addressed these problems with two experiments. First we investigated invertebrate populations in newly-installed turfgrass lawns and found that tilling compost into the soil as a pre-plant soil mitigation treatment increased the richness of invertebrate populations and did not negatively affect populations of detritivore organisms or their effect on thatch decomposition. We also found that yaupon holly, Ilex vomitoria, and tea, Camellia sinensis, were less susceptible to a key pest, tea scale (Fiorinia theae), compared with several of their more common ornamental congeners. Further, both native shrubs tested offer superior ecosystem services when considering their pest resistance alongside known benefits to wildlife compared to a non-native, more widely planted congener, Ilex cornuta

‘Dwarf Burford’. These two studies provide insights into more sustainable urbanization.

CHAPTER 1 LITERATURE REVIEW

Challenges Associated with Urban Landscapes

In recent years, urban landscapes have increased not only in great physical extent (Brown and Vivas 2005), but also in recognition as important study-systems due to their impact on surrounding ecosystems and the novel interactions that occur within them (Dale and Frank

2018). Over the past century, planet earth has experienced astounding human population growth, with current predictions of around 9.5 billion by the year 2050 (UN-DESA-PD 2015). In the early 2000s, over 50% of people lived in urban areas, and by mid-century it is expected that this will rise to 68% (UN-DESA-PD 2018). Perhaps the most striking prediction of population growth over the next few decades is that all of the world’s net population growth will occur in urban areas (UN-DESA-PD 2015). The southeastern United States is no exception. In fact, modeling predicts that as major cities in this region expand, the surrounding urban sprawl will continue to expand even more rapidly, connecting areas between cities with vast areas of low- density suburban development (Terando et al. 2014).

Florida has already experienced an explosion of population growth and development over the past half century, and current trends indicate that population will nearly double again by 2070 to over 33 million residents (FDACS et al. 2016). Current growth projections also indicate that if urban planning is not improved, nearly over one-third of Florida’s land area will be developed over this time, with an estimated 5 million additional acres converted to urban use (FDACS et al.

2016). These expanding urban areas will continue to be the driving force of environmental change to their surrounding local landscapes (Grimm et al. 2015). In light of this, focusing research on urban development, ecosystem services, and planning for sustainability will not only reveal the problems, but also the solutions for our future.

System I – Soil Mitigation for Lawns

Conditions typical of recently developed landscapes, including severely compacted soils and reduced organic matter, can increase plant stress and make recently installed plant material more susceptible to pests, further exacerbating maintenance requirements (Craul 1985, Watson and Koeser 2008, Loper et al. 2010). This carries to turfgrass lawns, which are frequently attacked by herbivorous insect pests that not only reduce the ecosystems services provided by lawns, but also result in increased pesticide use, natural resource waste, and costly repair (Held and Potter 2012, Thompson and Kao-Kniffin 2017). Thus, it is important to identify strategies we can use to maintain the beneficial functions and sustainability of lawns.

Benefits and Challenges Associated with Urban Landscapes

It is well-understood that plants in urban landscapes provide a multitude of beneficial services including aesthetic enhancement, recreation, carbon and nitrogen storage, environmental cooling, and air and water filtration (Beard and Green 1994, Raciti et al. 2011, Gómez-

Baggethun et al. 2013). Research over recent decades has uncovered many novel effects of urban development on plants and insects (Raupp et al. 2010, Dale and Frank 2018), but also strategies for developing more sustainable urban landscapes (Dale et al. 2016). In addition to physical and environmental benefits, residential landscapes in urban areas are also intimately associated with a growing proportion of people and play a significant role in building personal relationships between homeowners and their local natural environment (Gross and Lane 2007).

Unfortunately, many efforts intended to improve urban landscapes, such as large-scale tree plantings, irrigation reduction, and xeric or native plant drives, may fall short of their potential if the belowground health of ornamental plants is compromised by poor soil conditions

(Watson and Koeser 2008). Plants may be predisposed to a variety of widespread stresses, as

urban development often removes vegetation and topsoil, compacts subsoils, alters water flow, and negatively affects the organisms that live there (Day and Bassuk 1994). Recently developed urban and residential landscapes typically require significant maintenance inputs in the form of irrigation, fertilization, pesticide applications, and labor to encourage plant establishment and success (Barnes et al. 2018). Moreover, herbivorous insects are frequently more abundant and damaging in urban than surrounding natural areas (Raupp et al. 2010). Management of turf pests has traditionally relied on the use of conventional, synthetic insecticides since these products are relatively inexpensive, fast-acting, and may be applied preventatively with residual activity

(Larson et al. 2017). Important aspects to consider in this context include the conservation of predatory and parasitic organisms by encouraging the use of selective, reduced-risk or biorational insecticides rather than broad-spectrum products. It is also critical that cultural control practices are put into place to promote ecosystem health that encourage populations of beneficial organisms, including detritivores and natural enemies of pests.

Soil Mitigation Strategies

One affordable approach to improve soil quality for plants and other organisms in disturbed landscapes is by incorporating organic matter, such as compost or other topdressing

(Craul 1985, Lusk and Toor 2008). Composting is the process of transforming organic matter into an environmentally safe and stabilized organic amendment by intense microbial decomposition (Senesi and Brunetti 1996). Increasing organic matter has been shown to provide many benefits to soil physical structure, including increased aggregation, porosity, water infiltration, electrical conductivity (EC), and bulk density (Davey 1996, Cogger 2005, Loper et al. 2010, Olson et al. 2013). Organic matter also influences many biotic functions of the soil food web, such as promoting growth of mycorrhizal fungi and increasing microorganism abundance

and diversity, which in turn can reduce abundance of plant-parasitic nematodes (Muller and

Gooch 1982, Akhtar and Malik 2000).

In our study system, a commercial product known as Comand® Compost (produced by

Harvest Quest) was the source of organic matter amendment. Comand® is an increasingly popular commercial compost applied to residential lawns and is advertised as providing a wide range of benefits. These include high quality organic matter, improved water-holding capacity and infiltration, improve nutrient retention, increase microbial activity, and improve soil structure. Thatch reduction is also advertised, which is the subject of our Experiment 2.

Comand® consists of composted yard wastes and horse stall bedding. It is inoculated with an

HQ Bio Catalyst to initiate composting and subjected to a “reverse” composting process whereby heat moves inward (Jones 2018). Importantly, analysis of the inoculant product by the

Environmental Quality Laboratory at Colorado State University found that 13% of the fungal composition was the fungal class Orbiliomycetes, known as nematophagous fungi, and the largest group of bacteria were the Actinomycetales, known for decomposing chitin and cellulose

(Jones 2018). These and other components of biodiverse compost may have implications for nematode populations, or the decomposition of organic matter. The product can be tilled into the topsoil or spread over the ground or lawn as a top-cover treatment. Landscape managers need to know what benefits soil mitigation treatment with this product offer for establishment of landscape plants and long-term benefits to the soil.

System II – Shrub Selection

Woody ornamental plants provide a multitude of valuable services to the ecosystem and human residents of urban and residential landscapes (Bolund and Hunhammar 1999, Dunnett and

Qasim 2000, Chalker-scott 2015). Unfortunately, they are frequently attacked by herbivorous

insect pests, reducing their services and increasing maintenance inputs (Raupp et al. 2010).

Among the most effective and sustainable integrated pest management solutions in urban landscapes is proper plant selection to avoid key pest attack (Raupp et al. 1992). In Chapter 3, we test the relatively susceptibility of six woody ornamental plant species within the known host range of a key pest of ornamental plants. Here, we provide additional system information about this key pest, Fiorinia theae, and its management, then further describe the potential of alternative plant species, Camellia sinensis and Ilex vomitoria, which our results suggest may provide additional benefits in residential landscapes compared to several of their conventionally used ornamental congeners, Ilex cornuta ‘Dwarf Burford’, Ilex opaca, Camellia sasanqua and

Camellia japonica.

Tea Scale: an Armored Scale Insect Pest

Armored scales (Hemiptera: Diaspididae) are the most abundant scale insect family with

2,624 species in 426 genera currently recognized globally (García Morales et al. 2016). This group includes many of the most widely distributed and economically important pests of woody plants, with some estimated to cause over $2 billion in economic losses in the U.S. annually

(Kosztarab 1990, Miller and Davidson 2005). Scale insects may outbreak in response to urban landscape characteristics like urban heat islands (Meineke et al. 2013), broad spectrum insecticide applications (Raupp, Shrewsbury, et al. 2001), or reduced natural enemies (Tooker and Hanks 2000). One of these pests, tea scale (Fiorinia theae Green) is an exotic but long- established species that is widely distributed in the southern half of the United States (Miller

2016). Like most armored scales, tea scale is polyphagous, with plant host records from at least

14 genera in 12 families (García Morales et al. 2016). This pest is known as one of the ten most important scale insects in North and Central Florida nurseries (Dekle 1965), one of 43 serious

armored scale pests overall (Beardsley and Gonzalez 1975), and a serious world pest (Miller and

Davidson 1990). Within its host range, tea scale is most commonly encountered on Camellia and

Ilex spp. (Kuitert and Dekle 1972, Munir and Sailer 1985, Miller and Davidson 2005) and is best known as the most destructive pest of ornamental Camellia spp. in the United States (English and Turnipseed 1940, Kouskolekas and Self 1973, Trehane 2007).

In addition to ornamental Camellia spp., tea scale has long been reported to attack C. sinensis in the Southeast region, including Florida (Sasscer 1912, Nagarkatti et al. 1979).

Surprisingly, tea scale is not an important pest of C. sinensis tea crops in its native range (Das and Das 1962) nor is it problematic on wild C. japonica in Japan (Nagarkatti et al. 1979). The stark contrast in pest importance between regions where tea scale occurs is credited to an abundant natural enemy complex in its native range, which keeps tea scale populations below damaging levels – provided that the indiscriminate use of broad-spectrum insecticides is avoided

(Nagarkatti et al. 1979, Nagarkatti and Jayanth 1981). While several natural enemies that attack tea scale are present in North America (Munir and Sailer 1985, Cooper and Oetting 1987), their combined effect is considered insufficient to provide adequate control, and introduction of new parasitoids has been unsuccessful (Munir 1980). The importance of tea scale in North America is thus consistent with the supposition that armored scale insects are most destructive when introduced to novel environments in enemy-free space (Miller et al. 2005).

Host choice of tea scale has been described as erratic (Nagarkatti et al. 1979) and evidence of varietal level host susceptibility is scarce for Diaspidids in general (Beardsley and

Gonzalez 1975). Of the limited reports that exist, Kouskolekas and Self (1973) suggest no observable differences in susceptibility between several C. japonica varieties, and other studies lack recorded observations describing resistance. A single notable exception appears to be the

widely planted Burford hollies (i.e., Ilex cornuta ‘Burfordii’ and ‘Dwarf Burford’). Within the genus Ilex, the Burford hollies are consistently mentioned in association with severe infestations of tea scale as an economic pest (Kuitert and Dekle 1972, Gilman and Watson 1993, Hesselein et al. 1999). In contrast, only one record could be found that mentions a severe infestation on I. opaca (Plant Pest Control Division 1963), and reports mentioning I. vomitoria lack specific susceptibility descriptions altogether (Howell and Ramona 1973, Galle 1997, Gilman and

Watson 2014).

Tea Scale Management

Scale insects damage plants by extracting nutrients, leading to canopy dieback, leaf drop, and eventual plant death. Although tea scale infestations occur on leaf undersides and may be cryptic, homeowners and landscape managers generally have low thresholds for pest damage, taking action when 10-25% of a plant is visually affected (Raupp et al. 1988, 1992, Coffelt and

Schultz 1990). Wholesale nursery professionals may be more tolerant of aesthetic plant damage, but retail nurseries may have a similarly low tolerance of aesthetic injury due to customers’ disproportionate expectations of aesthetic appearance and relationship to plant value (Raupp et al. 1988). Therefore, in an effort to control pests and reduce plant damage, homeowners and professionals frequently resort to insecticide applications (Raupp et al. 1988).

Tea scale is a perennial management concern in both nursery settings and landscape plantings (Kouskolekas and Self 1973, Hesselein et al. 1999). Around 50 years ago, tea scale control was heavily reliant on organophosphate and carbamate insecticides, most of which have either been phased out or restricted and no longer available for residential or non-agricultural use. Recommendations for effective treatments once included aldicarb, high-rate soil applications of dimethoate, carbofuran, and phorate (Kouskolekas and Self 1973); various foliar

applications or undiluted trunk applications of dimethoate, oxydemeton-methyl, acephate, diazinon, and mixtures of summer oil with malathion or ethion (Kuitert and Dekle 1972,

Vaughan et al. 1976). Later, control options shifted towards the remaining organophosphates (i.e. acephate, malathion) and newer options from the pyrethroid and neonicotinoid (i.e. acetamiprid, dinotefuran) chemical classes, as well as insect growth regulators, including buprofezin and pyriproxyfen (Raupp et al. 2001, Rebek and Sadof 2009, Cloyd and Bethke 2011, Frank 2012).

In recent years, scale insect management has again shifted towards EPA reduced-risk insecticides, which are intended to provide adequate control with fewer negative effects via greater pest selectively, minimal non-target toxicity, and shorter persistence in the environment

(EPA 2018). When armored scale management is deemed necessary, efficacy trails targeting armored scales (Nielsen 1990a, Frank 2012, Xiao and Arthurs 2016, Xiao et al. 2016, Quesada and Sadof 2017) and IPM-based nursery recommendations (Braman et al. 2015, Knox et al.

2017) support the use of these products, including biorational insecticidal soaps and horticultural oils, insect growth regulators, anthranilic diamides, spinosyns, and sulfoximines. Despite these advancements, effective tea scale control remains difficult, especially as tea scale is multivoltine with overlapping generations and year-round crawler emergence, and prefers to colonize the underside of mature leaves within a plant canopy (Munir and Sailer 1985).

When considering edible plants (C. sinensis and I. vomitoria) that may be attacked by tea scale or other armored scale species, further research of insecticide options is needed. Systemic or translaminar products effective for scale insect control on ornamental shrubs may not be labeled for use on plants intended for foliage harvesting and tea or tisane production. Due to their status as minor crops, little research has examined pest management on tea crops in the continental United States. Therefore, there is a need to evaluate reduced-risk products that are

labeled and appropriate for tea scale control on consumable plants in both production and landscape environments. Despite this need, identifying key pests and gauging the relative susceptibility of host plants is critical for developing IPM programs.

Camellia sinensis: Potential in the Landscape

Camellia sinensis (L.) Kuntze, best known as tea, is a broadleaf evergreen shrub belonging to the family Theaceae. The true native range of tea is unknown, but domestication has historically been centered in India and China. The ornamental species, Camellia japonica and Camellia sasanqua, are widely planted in the southeastern United States, but on a worldwide scale, tea is by far the most economically important Camellia sp. Leaves are harvested to produce the second most-consumed beverages worldwide (Chang 2015), with 2018 production estimated at 5.8 million metric tons (Deutscher Teeverband 2020). Annual United States tea production is estimated at a modest 700 kg of tea, grown on 181 hectares in 17 states, with the greatest portion of growers in Hawaii (Pettigrew 2018). In the Southeastern United States, growing interest in tea for intercropping or alternative crop and garden diversification has driven several breeding and varietal selection efforts (Orrock et al. 2017, LeCompte 2018).

Tea grows naturally into a small understory tree, but is typically formed into the characteristic low hedge in sun or part-shade by a critical series of pruning measures in the first

3-5 years after planting (Bezbaruah and Barbora 1983, Manivel 1998). Once established and pruned to the desired form, the shrubs are considered low maintenance and can have extraordinarily long life spans of 50-80 years in production (LeCompte 2018). Although the process of tea-making is an additional skill in itself, the novelty of growing tea in the home landscape may be an attractive form of landscape engagement, especially in the wake of popular trends in edible residential gardening (Conway 2016). Tea cultivation in the residential landscape

does hold some challenges. Chief among these is a foliar anthracnose disease (Colletotrichum species complex), which is the subject of additional ongoing research at the University of

Florida. Several other arthropods present potential risks to tea in the region and may require further work, including a peacock mite (Acari: Tuckerellidae: Tuckerella japonica Ehara) (Achor et al. 2017), and chilli thrips (Thysanoptera: Thripidae: Scirtothrips dorsalis Hood), which is also known as yellow tea thrips in tea-producing regions (Hazarika et al. 2009).

Ilex vomitoria: Potential in the Landscape

Ilex vomitoria Aiton, commonly known as yaupon holly, is a dioecious, evergreen shrub in the family Aquifoliaceae. Yaupon is native to the southeastern United States with a range stretching along the coastal plain from the southeast corner of Virginia, south to central Florida, and west to Texas (USDA-NRCS 2019). It is tolerant of a wide range of soil types, sun exposure, and environment types. It commonly grows as an understory shrub in hardwood forests and pinelands (Palumbo et al. 2007). However, it is tolerant of dry to fairly wet soils as well as salt spray, and can be found near brackish and salt marshes, sand dunes of coastal areas, maritime forests (Immel and Anderson 2009). Yaupon is considered one of the toughest hollies, transplants well, and is highly appropriate for urban landscape plantings (Immel and Anderson

2009, Shadow 2011). Previous research has also demonstrated that the species does not need additional irrigation in the Florida climate, making it appropriate for gardens attempting to reduce irrigation (Scheiber et al. 2008). Indeed, the adaptability and vigor of yaupon has generated some concern for weedy potential on the margins of its native range (Schnelle 2019).

Approximately 17 cultivars are marketed, including forms desired from other Ilex spp. cultivars, such as dwarf and hedging, columnar, and weeping forms (Galle 1997, Palumbo 2006).

For centuries, native tribes throughout the region not only revered the stimulating beverage

produced from its leaves and twigs, but likely transplanted plants for cultivation in new areas

(Hammett 1992). Early Spanish colonists in Florida quickly adopted the beverage, followed by

English colonists in the Carolinas, however, unlike true tea, the consumption of yaupon declined and its history was largely forgotten (Hudson 1979, Palumbo et al. 2009). The beverage gradually fell from common use until the American Civil War, when it enjoyed a brief return to popularity due to the scarcity of other caffeinated beverages (Hudson 1979, Wainwright and Putz

2014). However, unlike tea, yaupon eventually became established in the ornamental plant trade.

Despite excellent tolerance for a wide range of uses and habitats and a long history of use, few people recognize the plant as the same species historically harvested from the wild and used to brew a caffeinated tisane (a hot, tea-like beverage). Thus, the edible qualities went largely unnoticed by the public until a recent resurgence of interest sparked yaupon tisane production in several southern states. In Florida, commercial producers have enjoyed widespread interest and collaboration requests from the health and alcoholic beverage industries (kombucha and beer), from growers wishing to diversity their crops, and even a re-established market in overseas exports (Bryon White, personal correspondence). This momentum holds opportunity to reevaluate the function and services of yaupon holly in a landscape setting.

Yaupon has remarkably few pest and disease concerns. Leafminers (Diptera: Phytomyza spp.) are an occasional nuisance pest (Johnson and Lyon 1991, Immel and Anderson 2009), as is the yaupon psyllid, Gyropsylla ilicis (Mead 1983). This psyllid produces leaf galls on new growth in late winter and early spring, but galling causes no significant damage to overall plant health and often goes unnoticed (Johnson and Lyon 1991). Additionally, while galling may be a minor concern to observant growers and buyers, the popular small-leaved dwarf cultivars commonly traded as ornamentals are very rarely attacked (Mead 1983). In addition to tea scale,

several other armored and soft scale insects are recorded from yaupon (Dekle 1965, Hamon and

Williams 1984), but there are no recorded pests or diseases of significant economic or aesthetic importance (Immel and Anderson 2009) at this time.

Summary of Other Plant-Ecosystem Interactions

There is growing evidence that plant selection should consider species-specific traits that enhance multiple aspects of ecosystem services, such as floral resource availability, refugia for natural enemies, and benefits to wildlife (Parsons et al. 2020). Chapter 3 of this thesis focuses on key pest resistance as a broadly desirable trait; however, these other aspects of ecosystem services should be considered alongside pest resistance when designing functional and sustainable ornamental plantings and may even be a priory for some gardeners. Limited information is available for the following topics but serves as a starting point for questions we have received from interested growers of C. sinensis and I. vomitoria.

Resources for pollinators. There is limited specific information describing benefits to pollinators from Ilex and Camellia spp. Ilex sp. are generally considered excellent floral resources. Bloom duration lasts from around 10 days to several weeks and bloom periods differ by species, ranging approximately from early (I. cornuta), mid (I. vomitoria) to late (I. opaca) spring (Galle 1997, Miller and Miller 2005). As a dioecious group, male and female plants are required to provision both pollen and nectar resources as well as fruit production. An exception is I. cornuta ‘Dwarf Burford’, which is exhibits parthenocarpy and can produce fruit with infertile in the absence of pollination (Carr 1991, Galle 1997). To our knowledge, none of the

Ilex spp. in this study provide clear resource superiority other others; therefore, plant size and sex may be greater determinants of resource benefit. For example, male I. opaca produce up to 7 times more flowers than female trees (Carr 1991), but female flowers produce nectar and

resulting fruit. In addition, our observations suggest that the nectar-producing female flowers are attractive to a wide range of insects beyond pollinators, including ladybeetles and several flies. In contrast, Camellia sp. are not typically planted for pollinator resource value. Ornamental

Camellia sp. are hybridized, and certain double flower forms may provide fewer resources than simple flowers, such as those with wild type flowers, including C. sinensis (Li et al. 2017).

Observations of field-grown C. sinensis in Central Florida suggest that the floral resource-rich flowers are attractive to honeybees and Lepidopterans (Orrock 2018, personal correspondence).

Although the flowers of C. sinensis are smaller and less valued compared to more traditional ornamental species, their floral resources value may hold priority over aesthetic value for some homeowners and landscape developers.

Resources for wildlife. In addition to pollinator services, resources for other wildlife are an important function of residential landscapes. For many landowners, watching or attracting wildlife is a major priority, on par with recreation and entertainment value (Goddard et al. 2013).

For example, Lepczyk et al (2004) found that over 50% of homeowners intentionally planted and maintained vegetation for birds, and 45-64% carried out other activities to support birds, such as feeding birds and providing bird houses. The ecosystem services provided to bird populations may be most important in light of the severe losses in both abundance and diversity observed in

North American bird populations over recent decades (Rosenberg et al. 2019). Unfortunately, interactions between non-native Camellia and North American wildlife are poorly documented.

However, ample records of benefits from Ilex spp. are available, with a focus on the native species and value to birds. Both native and exotic Ilex spp. produce fruit that are important resources for birds during winter when many other food become scarce (McPherson 1987). For example, the fruit of I. vomitoria is fed upon by at least 28 reported bird species in the Southeast,

in addition to providing value nesting and roosting cover for numerous species, including coastal birds (Martin and Mott 1997). Similarly, at least 18 species are reported to feed on fruit of I. opaca (Coladonato 1991). However, there is some evidence that I. cornuta fruit are less preferable than I. vomitoria. McPherson (1988) found that frugivorous waxwing birds

(Bombycilla cedrorum) preferred native I. vomitoria fruit 23% more than I. cornuta in lab studies, but when given many available options in field studies, I. vomitoria was the most preferred while I. cornuta was seldom eaten. Several factors may influence fruit preference, including favoring smaller fruit size, where I. vomitoria fruit average 7.05 mm in diameter compared to 9.82 mm for I. cornuta (McPherson 1988). Additionally, plant height is often a determining factor in foraging preference, likely for a higher vantage point and safety from predators (Best 1981, Skeate 1984). Thus, since Ilex spp. value to birds is associated primarily with fruit-bearing female plants, there is a need for market-accessible female cultivars that offer a range of forms desirable in the landscape. Currently, the most common I. vomitoria dwarf types are either non-fruiting male (‘Schillings Dwarf’) or rarely-fruiting female (‘Nana’) cultivars. Wider commercial availability of a female cultivar similar in form to ‘Dwarf Burford’ may encourage adoption while providing greater benefits compared to male dwarf cultivars.

Although birds are a prominent concern, other animal groups are also commonly associated with the residential landscapes. Of the native Ilex spp. in the southern United States, I. vomitoria is considered the most beneficial to wildlife due to the fruit and thicket-like growth providing nesting and cover habitat (Halls and Ripley 1961, Martin and Mott 1997). In addition to their importance for many bird species, the fruit of both I. vomitoria and I. opaca are sought after by deer and a variety of small mammals common in urban areas, such as squirrels and racoons (Coladonato 1991, Martin and Mott 1997). I. vomitoria foliage is an important browse

source for white-tailed deer (Goodrum and Reid 1958, Martin and Mott 1997) but is also highly tolerant of defoliation (Lay 1957). Conversely, other ornamental Ilex spp., including I. opaca and

I. cornuta, are much less preferred for deer browsing (Conover and Kania 1988). Based on available information, I. vomitoria and I. opaca provide the greatest ecosystem services to wild of the plants tested in this study.

Research Objectives and Thesis Structure

In the context of rapidly expanding urban landscapes and the benefits healthy urban plants provide, the goal of this thesis was to evaluate methods to enhance landscape sustainability and functionality. This thesis is divided into four chapters. Chapters 1 and 4 provide an introduction and conclusion to the body of work, while chapters 2 and 3 will be published as separate peer-reviewed research publications. In Chapter 2, our objective was to investigate the effects of tillage and compost as part of the residential landscape creation process, asking how such practices influence invertebrate reestablishment and associated ecosystem services. Specifically, we (1) surveyed the abundance and richness of lawn-dwelling invertebrate functional groups, (2) determined abundance of detritivore taxa and their associated thatch decomposition services, and (3) evaluated taxa important for biological control, including soil- dwelling entomopathogenic nematodes. In Chapter 3, we investigated the potential for two underutilized shrubs to provide benefits of key pest avoidance and multifunctionality compared to their conventional ornamental congeners. To do this, we (1) evaluated six native and exotic landscape shrub species for susceptibility to tea scale, and (2) compared damage caused by the tea scale infestations. Ultimately, we hope that both projects will help site developers, nursery growers, landscape managers, and homeowners create and maintain more sustainable urban landscapes in Florida and the southeastern United States.

CHAPTER 2 EFFECTS OF SOIL MITIGATION PRACTICES ON TERRESTRIAL INVERTEBRATES FOLLOWING RESIDENTIAL DEVELOPMENT

Abstract

Residential areas are the most rapidly expanding land use type in the Southeastern United

States. The residential development process impairs soil functions primarily through compaction and the removal of topsoil and natural vegetation, which results in reduced water retention, infiltration, and root penetration, and can inhibit establishment of newly installed turfgrass and ornamental plantings. Plant stress reduces growth and increases vulnerability to pests, often leading to supplemental management inputs in the form of water, fertilizer, pesticides, and labor.

Soil-dwelling invertebrates, including detritivores and natural enemies of pests, provide valuable services that may facilitate plant establishment and reduce plant injury and maintenance inputs.

However, disturbance during development likely reduces the services provided by soil-dwelling invertebrates, although it is poorly understood. This study compares the effects of two soil mitigation tactics, tillage and compost application, on invertebrate communities recovering after disturbance and the services these invertebrates provide in residential landscapes. We focus on the relationships between detritivores and thatch decomposition rates, between entomopathogenic nematodes and a key turf insect pest (hunting billbug), and the overall abundance of arthropod herbivores and predators. We found that tillage and compost showed unexpectedly mediocre benefits during the first year, although positive effects on invertebrates became more evident during the second year. As expected, time remained the most significant recovery factor. Ultimately, these results can inform more sustainable residential development and landscape maintenance practices as we strive for proactive ecosystem health restoration in highly disturbed urban landscapes.

Introduction

In recent years, research and education efforts have driven public awareness and action towards more sustainable urban landscapes and proactive ecosystem management (Watson and

Koeser 2008). For example, community efforts such as large-scale tree plantings, fertilizer ordinances, irrigation reduction policies, and xeric or native plant drives (Peper et al. 2007,

Dukes et al. 2008, Hartman et al. 2008, McPherson et al. 2008). However, these initiatives can fall short of their goals if soil health and functioning is compromised (Watson and Koeser 2008), which is commonplace in urban and recently developed suburban landscapes (Cogger 2005,

Watson et al. 2014). Urban development often removes native vegetation and topsoil, disrupts and compacts subsoil structure, alters water flow, and negatively affects the organisms that live there (Craul 1985, Gregory 1991, Scheyer and Hipple 2005). In result, soil contamination, mechanical resistance, and insufficient or excess soil moisture impair plant root growth and function in water and nutrient uptake (Watson et al. 2014). Moreover, the replacement of natural habitat with residential homes and human-selected vegetation significantly changes the arthropod community inhabiting it (McKinney 2002), which reduces or alters the ecosystem services they provide (e.g., nutrient recycling and redistribution, decomposition, pollination, biological control) (McIntyre et al. 2001, Tresch 2019).

One approach to improving soil quality for plants and other organisms in disturbed landscapes is by incorporating organic matter, such as compost, into the soil (Lusk and Toor

2008). Composting is the process of transforming organic matter into an environmentally safe and stabilized organic amendment through intense microbial decomposition (Senesi and Brunetti

1996). Increasing organic matter provides many benefits to soil physical structure, including increased aggregation, porosity, water infiltration, and bulk density, and influences many biotic functions of the soil food web, such as promoting growth of mycorrhizal fungi and increasing

microorganism abundance and diversity (Davey 1996, Cogger 2005, Olson et al. 2013).

Additionally, some of the microorganisms in the applied organic matter reduce abundance of plant-parasitic nematodes (Muller and Gooch 1982, Akhtar and Malik 2000). In our study, we apply a treatment of compost and tillage to both reduce surface compaction and amend the topsoil with composted organic matter. Although tilling has been observed to improve water infiltration of compacted soils by twofold, tillage with the addition of compost has increased infiltration by fivefold (Olson et al. 2013).

In addition to the physical characteristics of soils, there are many soil and lawn-inhabiting organisms that directly affect lawn ecosystem functioning and the health of plants living in it

(Bray and Wickings 2019). Some of these organisms are detritivores affecting thatch, a layer of organic material on the soil surface derived from grass clipping and senescent leaves, which can reduce beneficial nematode movement (Georgis and Gaugler 1991), pesticide penetration and efficacy, pest suppression, and nutrient cycling (Potter et al. 1990). Several soil and lawn- dwelling invertebrate groups provide valuable decomposition services that help recycle nutrients and prevent the over-accumulation of dead plant material in the thatch layer (Potter et al. 1990,

Wickings et al. 2012). Unfortunately, detritivore communities can be negatively affected by the loss of topsoil organic matter and the associated stabilized moisture, temperature, and vegetation

(Eaton et al. 2004). Treatments that restore organic matter may have a positive influence on thatch decomposition rates and nutrient recycling by improved habitat for recovering detritivore populations.

Turfgrass lawns are frequently attacked by herbivorous insect pests, which reduce the ecosystems services provided by lawns, but also result in increased pesticide, natural resource, and monetary inputs (Held and Potter 2012, Thompson and Kao-Kniffin 2017). Conditions

typical of recently developed landscapes, like severely compacted soils and reduced organic matter, can increase plant stress and make recently installed plant material more susceptible to pests, further exacerbating maintenance needs (Craul 1985). Thus, it is important to identify strategies to increase the resilience of recently-installed lawns to insect pests. The hunting billbug, Sphenophorus venatus vestitus (Coleoptera: Curculionidae), is the most damaging and abundant Curculionid pest of warm-season turfgrasses in the southern United States, particularly zoysiagrass (Poaceae: Zoysia spp.) (Huang et al. 2014), with both adults and subterranean grubs causing damage (Johnson-Cicalese et al. 1990). Fortunately, naturally occurring nematodes, especially Steinernema sp. and Heterorhabditus sp. (Nematoda: Steinernematidae and

Heterorhabditidae), can control several important soil-dwelling turf pests, including billbugs. In one case, entomopathogenic nematodes have reduced turfgrass pest populations to the extent of saving over $10 million in annual pest-associated costs (Mhina et al. 2016). Although improved soil conditions are likely to benefit entomopathogenic nematodes, we have a poor understanding of such effects from tillage or compost in residential landscapes.

Some form of soil mitigation post-development, but before plant installation, is likely to affect soil and lawn-dwelling organisms and facilitate recovery of residential landscape ecosystems. Identifying the most effective strategies may reduce short- and long-term maintenance inputs, but also increase the ecosystem services provided by residential lawns. To determine the effects of multiple soil mitigation tactics, we monitored the recovery of soil and lawn-dwelling invertebrates and their associated ecosystem services for two years in a recent residential development where multiple soil mitigation treatments were integrated prior to plant installation. We first test the hypothesis that with increasing soil mitigation efforts, the abundance and richness of beneficial surface-dwelling invertebrates (e.g., predators, parasites,

detritivores) will increase. Second, we further investigate surface dwelling invertebrates by testing the hypothesis that ecosystem functioning associated with detritivores (i.e., thatch decomposition) would also increase with increasing soil mitigation efforts. Finally, we investigate the effects of soil mitigation practices on soil-dwelling entomopathogenic nematodes and the biological control services they provide, testing the hypothesis that increasing soil mitigation efforts will be associated with reduced nematode activity.

Materials and Methods

Study Site

Site history can be an important factor when evaluating urban ecosystem services, especially those relating to soil or soil-vegetation interactions (Ziter and Turner 2018). Some research indicates that this is particularly important for lands converted from agricultural use to urban residential use (Raciti et al. 2011). Our study site was located at On Top of the World

Communities, a 55+ retirement village located in Ocala, a small city in central Florida. The property was originally developed in the 1930s into a 9,000-acre working cattle ranch by the

Norris Cattle Company, based in Chicago, Illinois. The land was predominantly Pensacola bahiagrass (Paspalum notatum Flueggé) pastureland, with large portions rotated through crops of peanut, winter wheat, and Alyce clover. In 1975, Mr. Sidney Colen purchased 13,000 acres, including the Circle Square Ranch, from the Norris Cattle Company and began developing part of the land into the current retirement community, golf courses, and managed natural areas

(Leonard 2013, Colen 2014).

Experimental Design

During November of 2015, a model-home residential development was initiated, beginning with soil grading, compaction, and soil horizon alteration, in a long-disused pastureland between agricultural fields. The newly constructed neighborhood was partitioned into eleven lots, each approximately 1000 m2 (ca. quarter-acre lots) and containing a single- family home averaging 140 m2 (1500 ft2) with a front and back lawn. Prior to landscape plant installation, each lot was assigned a treatment in a randomized complete block design and blocked according to pre-existing soil physical characteristics (Figure 2-1). Immediately following construction in early 2017, but prior to landscape plant installation, one of three soil mitigation treatments were implemented in the front and back yards of each lot, resulting in six replicates of each treatment.

In treatment 1, henceforth referred to as no-till, we left the soil unamended and compacted as a result of the construction and grading process (Figure 2-2). This treatment functions as our control and standard development practice. No portion of the neighborhood was left undisturbed during development that could have functioned as a separate, true control representative of the original site. For treatment 2, henceforth referred to as tillage, we tilled the soil to a depth of ca. 15 cm (6 in), reducing the surface compaction but not altering the soil composition. Treatment 3, henceforth referred to as tillage + compost, included the application of a commercial compost at a rate of about 3 m3 per 93 m2 (4 yd3 per 1000 ft2). This is equivalent to approximately 3.2 cm (1.3 inch) depth at a cost of $11.12 per m3 of compost. The compost was then tilled into the soil to a depth of 15 cm (6 in).

The compost product (Comand® by Harvest Quest) is made primarily of composted yard wastes and horse stall bedding. During the composting process, the organic material is inoculated several times with a microbial catalyst and re-inoculated with mesophilic organisms after the

thermophilic phase is complete, steps intended to create a diverse microbial community (Jones

2018). Importantly, analysis of the inoculant product by the Environmental Quality Laboratory at

Colorado State University found that 13% of the fungal composition was the fungal class

Orbiliomycetes, known as nematophagous fungi, and the largest group of bacteria were the

Actinomycetales, known for decomposing chitin and cellulose (Jones 2018).

Immediately following implementation of the soil treatments, ‘Empire’ zoysiagrass

(Zoysia japonica Steud) sod and ornamental grasses, shrubs, and small trees, were installed on each property (Figure 2-3). For the duration of this study, groundskeeping staff managed the lawns of all plots, including standardized mowing, slow-release granular fertilizer applications, broadleaf herbicide spot-treatments, and fungicide applications. Some insecticide use, including clothianidin and chlorantraniliprole, was applied immediately after landscape installation, but was halted before sampling began. Due to miscommunications with the grounds crew, we do not yet know the exact dates or formulations of applications.

Survey of Lawn-dwelling Invertebrates

To survey invertebrates living in the lawns and primarily inhabiting the turfgrass, we performed a series of pitfall trapping. We deployed four 30 mm diameter plastic vials (50 mL

Falcon™ Conical Centrifuge Tubes, Corning, New York, USA) filled halfway with 20% propylene glycol-detergent solution in the front and back lawn of each lot (4 per lawn, 8 vials per lot). We left the pitfall traps in the lawns for 7 days, then removed them and transferred their contents to 70% ethyl alcohol for storage until later examination using dissecting microscopes.

Sampling was done every two months from April to October of 2017 and 2018. We identified specimens to several taxon ranks based on their functional group as detritivores, predators, or herbivores. Specifically, identification levels included the following: class (Entognatha,

Chilopoda, Diplopoda, Gastropoda), subclass (Acari), order (Oribatida, Aranae, Dermaptera,

Orthoptera, Coleoptera, Diptera, Thysanoptera, Hymenoptera, Lepidoptera, Hemiptera) and family level for prominent groups of diverse orders (Staphylinidae, Curculionidae, Formicidae, and several Hemipteran families).

Quantifying Detritivores and Thatch Decomposition

Detritivore populations were measured using the pitfall-trap survey described above. To compare the effect of soil mitigation treatments on decomposition, we used a modified litter bag technique (Potter et al. 1990) to mimic natural thatch accumulation and decay in the lots and loss-on-ignition analysis to quantify the amount of organic matter lost over time (Landschoot and

McNitt 1994, Wickings et al. 2012, Jones 2018). To mimic natural thatch, we obtained fraze mower clippings of ‘Empire’ zoysiagrass grown with standard maintenance practices. Clippings were dehydrated at 60 °C for 3 hours in a commercial drying oven and then sifted to remove any soil. Five 20 g samples of desiccated clippings were set aside as controls and stored at room temperature in sealed plastic bags. We constructed 54 cages (5 × 5 × 25 cm) made of galvanized wire mesh (5 mm2 mesh openings). Each mesh cage was numbered, weighed, and packed with

20 g of desiccated clippings. Clippings that fell from each cage during packing and transportation to the field were also weighed to record an exact weight of material in each cage at the time of deployment.

Near the center of each back lawn, we installed six cages spaced 1 m apart on a 2 x 3 m grid, by cutting a narrow wedge into the turfgrass, removing soil, and inserting the thatch-filled cage, ensuring the cage was covered by the lawn turfgrass. We deployed cages in June 2017 and retrieved them in pairs at 3, 6, and 9-month intervals. After retrieval, we separated all partially decomposed litter from living zoysiagrass stolons, rhizomes, and roots that had grown into the

cages over time. The litter was transferred into paper sacks and dried at 60 °C for 2 days. After drying, litter was separated from mineral soil using a 1.15 mm sieve and a seed-blower

(Seedburo 757 Improved South Dakota Seed Blower, Des Plaines, IL, USA). The partially- decomposed samples and five undecomposed control samples were ground to a fine powder using a Cyclone Sample Mill (Udy Corp., Ft. Collins, CO, USA) and a 1 mm sieve, re-dried at

50 °C for 1 day, weighed, and stored in sealed vials prior to analysis. For the loss on ignition analysis, ten percent (by weight) of each stored sample was incinerated in a muffle furnace for at least 4 hours at 500 °C. The litter ash was weighed and subtracted from the pre-burn weight to determine mass of carbon-based litter. Litter mass lost from the partially decomposed samples was compared to that of the control samples and is reported as a percentage of litter carbon lost after each period of decomposition.

Entomopathogenic Nematode Biological Control

To quantify naturally occurring soil-dwelling entomopathogenic nematode (EPN) activity, we surveyed the soil profiles extracted from each front and back lawn in April, July, and

October of 2017 and 2018. For each lawn profile sample, we used a straight spade to remove a section measuring ca. 1350 cm3 (WLD: 15 x 5 x 18 cm). We then bagged and gently homogenized the rootzone soil, along with some thatch and turf, from half of each soil profile.

We retained 300 mL of this material and returned excess soil with replacement sand to fill each divot. Sample bags were labeled, transported in a cooler and stored at 4 °C until processing within 1-2 days. To evaluate EPN activity in each lawn sample, we used greater wax moth larvae

(Lepidoptera: Pyralidae: Galleria mellonella) as model host insects (Bedding and Akhurst 1975).

We placed 20 waxworm larvae in three 540 ml clear plastic tubs (6-7 waxworms per tub) and gently covered them with 100 ml of the sample soil material. We added distilled water to the tubs

as needed for consistent, slightly damp soil. The tubs were covered with perforated lids and stored in a dark room at 24 °C. After 3 days, the soil was turned out and each waxworm visually inspected. Dead or dying (discolored) waxworms were removed and placed in a White traps

(White 1927, Orozco et al. 2014). Live waxworms were returned to the tubs with soil. We repeated collection every 3 days for a total of 9 d of exposure. Each White trap was examined 5-

10 days later to determine if the cadaver had been internally colonized by EPNs. If nematodes emerged, they were divided and saved in separate vials of 90% ethanol and pure water. We used these data to calculate percent EPN infection due to exposure from each front and back lawn.

Statistical Analysis

We analyzed data using mixed-effects models treating block as a random effect. We examined the effects of treatment and sampling date on invertebrate population count data using one-way analysis of variance (ANOVA) with means separation by Tukey’s HSD test (P < 0.05).

All data were analyzed and figures generated using JMP Pro 14 (SAS Institute Inc 2019). Count data were log(x+1) or log10(x+1) transformed prior to analysis to increase the normality of residuals, with assumptions of normality examined using the Shapiro-Wilk W Test. We analyzed entomopathogenic nematode data using the mean percentage of wax moth larvae that became infected by exposure to the soil, examining effects of treatment and yard (front or back lawn) using one-way ANOVA as described above. Thatch decomposition was analyzed by the percent carbon lost at each sampling date using one-way ANOVA.

Results

Survey of Lawn-dwelling Invertebrates

Specimens collected in the pitfall traps placed in each front and back lawn were identified to functional group and higher taxon as previously described. Detritivores identified included collembolans, oribatid mites, millipedes, earwigs, flies, and molluscs. Herbivores included grasshoppers, crickets, mole crickets, thrips, true bugs, and weevils. Predators included rove beetles, ground beetles, earwigs, spiders, centipedes, ants, and other predatory or parasitoid

Hymenopteran groups. Rare exceptions to these functional groupings (e.g. a predatory thrips in the family Phlaeothripidae or predatory flies in the family Dolichopodidae) were noted during identification and reallocated to the appropriate functional group. Earwigs (Insecta: Dermaptera) were included as both predators and decomposers due to their typically omnivorous diet and relevant role in both functions (Albouy and Caussanel 1990).

Contrary to our hypothesis, overall arthropod abundance in April and June of 2017 was statistically lower in tillage and compost treatments than in plots with no-till or tillage alone

(Figure 2-4). This trend began to reverse during the summer, after which the tillage + compost treatment had higher abundance at 4 of 5 following sample dates. However, while the effect of treatment depended upon the sampling date (significant treatment x date interaction), the overall effect of treatment was not significant, thus, seasonality and time were the greater determinants of overall arthropod abundance (Table 2-1). Overall richness at the Order level followed a similar pattern, as we observed irregular population fluctuations until after the first summer

(Figure 2-5). After that point, not only did invertebrate richness increase over time, but we found a significant effect of treatment, supporting our hypothesis that the tillage + compost treatment would support the greatest arthropod richness, and no-till the lowest (Figure 2-1).

Detritivores and Thatch Decomposition

Detritivores represented the majority of individuals collected, consisting primarily of

Oribatid mites and Entognatha, which is consistent with similar studies of terrestrial arthropod community structure (McIntyre et al. 2001). We observed a general increase over time with large swings in seasonal variation during the first year, but more stable populations in the second season after disturbance. We also observed significant variability between treatments on 4 of 6 sampling dates (Figure 2-6), but no consistent effect of treatment overall (Table 2-1). The rate of thatch decomposition (as measured by amount of carbon loss) was similar across all treatments, averaging 43% after 3 months and 90% after 9 months. Thatch decomposition in the tillage + compost treatment had undergone slightly more decomposition at both 3 and 9 months; however, the difference was not statistically significant (Figure 2-7, Table 2-1).

Entomopathogenic Nematode Biological Control

White trapping wax moth larvae exposed to soils indicated that entomopathogenic nematodes occurred in all treatments and plots. Furthermore, variation in color of the wax moth larvae cadavers indicated that both major families of EPNs were present in all treatments, as

Steinernematid parasitism results in cadavers that are brown to ochre in color, while

Heterorhabditid parasitism causes cadavers to turn a brick red to dark purple color (Orozco et al.

2014). A significant effect of treatment was observed in parasitism levels (F82 = 3.55, p =

0.0311) (Table 2-1). Consistent with our, hypothesis that increasing mitigation efforts may be associated with reduced nematode activity, exposing larvae to soils from the tillage + compost treatment resulted in statistically less parasitism than the tillage treatment, but neither were statistically different from the no-till treatment, suggesting a negative effect of the compost

(Figure 2-8).

To capture any effects on turfgrass pests, we measured adult hunting billbug abundance using the pitfall traps. Hunting billbugs were the most abundant turfgrass pest found at our study sites. The low parasitism observed in the tillage + compost treatment was most evident during the October 2017 sampling date (13% compared to 30% and 38% in the no-till and tillage treatments, respectively), during which larval stages of hunting billbug are active in the soil, and thus vulnerable to EPN parasitism. Adult billbug populations showed no statistical difference between treatments during the first season; however, we found that the next generation emerging in the spring of 2018 were consistently most abundant in the tillage + compost treatment (Figure

2-9), suggesting an effect of EPN parasitism of billbug larvae in October 2017.

Our results indicate that arthropod predators were slow to recover during the first season, especially in the tillage and compost treatment (Figure 2-10). However, this pattern reversed during the second year, with the tillage + compost treatment numerically supporting the highest predator abundance of all treatments, although the overall effect of treatment was not significant.

Rove beetles (Coleoptera: Staphylinidae) were the most prominent predatory group observed and accounted for the majority of the spring 2018 population peak. Overall herbivore abundance (not presented) was examined and numbers were very low, following a similar trend as the hunting billbug population, which was the only major pest consistently found in the plots.

Discussion

Residential development and land use change is among the most pervasive and disruptive events going on throughout the U.S. As urbanization and global change drive biodiversity loss and affect the services plants and animals provide, gaining insight into these effects and how to mitigate them is critical (Thompson and Kao-Kniffin 2017). Our results suggest that time after disturbance was the most important factor for invertebrate abundance and richness recovery, but

that soil mitigation treatments showed some effects that were dependent on time. In particular, our data showed a general pattern of the tillage + compost treatment having similar or lower overall population abundance and richness than other treatments early in the survey period, but a pattern reversal as time progressed, becoming similar or higher than other treatments during the second year. For example, abundance of detritivores (the bulk of organisms collected) in the tillage + compost treatment was statistically lower than the other treatments at the beginning of the sampling period, but was consistently highest among treatments towards the end of the study.

One possible explanation for our observation that arthropods were initially least abundant in the compost treatment is that insecticide applications made during the early spring of 2017 were most persistent in soil with elevated organic matter, compared to the no-till and tillage treatments

(Adams 1973, Liu et al. 2006). We did not test for pesticide residues in the soil, but our results suggests that insecticide applications that negatively affect turf and soil fauna may have more persistent effects in the presence of organic matter originating from compost treatments (Peck

2009). Therefore, the benefits of applied soil organic matter may be reduced if persistent insecticides which bind to organic matter are also applied. We did observe an interesting trend indicating an undesirable effect of compost on trophic interactions, although this effect was also temporal and did not appear to translate to plant damage or maintenance inputs.

Despite differences among detritivore populations at several sampling dates, the overall population movement was more dependent on seasonality and time after disturbance than the effect of treatment. This is consistent with the results of our thatch decomposition experiment.

Attempting to draw further conclusions from this information is difficult due to the unknown role and activity of nutrient-cycling microbes in the compost treatment. For our purposes, these data

are of practical importance as it suggests that none of the treatments will cause unwanted thatch accumulation due to a strong negative impact on detritivore communities.

The surprising result that hunting billbug adult abundance increased with increasing levels of soil mitigation could have several explanations. The most likely possibility supported by our data is that the tillage + compost treatment reduced EPN activity, during the time of year when hunting billbug larvae were in the soil and exposed to EPN parasitism. If this is the case, nematode antagonists in the compost could have negative implications for pest management by suppression of EPN activity, as well as documented positive implications due to suppression of plant-parasitic nematodes (Jones 2018). Based on our result of similar EPN activity across treatments during the second October sampling date, we would not expect to see a reoccurring pattern with hunting billbug emergence that could cause a maintenance problem. However, this could be investigated further if composts having nematode-suppressive qualities are applied mor regular to turf as topdressings. A second potential explanation for increased hunting billbug abundance is that the mitigated soils supported healthier turfgrass lawns, which were more attractive to the weevils collected in pitfall traps. A more complete evaluation of these results will be possible after further discussion and integration of lawn health data from other collaborators working in this same study site.

In summary, our results suggest that the tillage + compost treatment, although highly dynamic, was associated with beneficial trends over time, while tillage alone had no consistent benefit for invertebrate populations. The strongest positive effect of treatment was observed in higher taxa richness, with tillage + compost showing the most benefit of increased richness during the second season. The greatest negative effect of treatment was observed in hunting billbug population, which we suspect is linked to decreased EPN activity in the compost-

amended soil. Overall, we found that compost + tillage may provide benefits of increased invertebrate richness and moderate increases in abundance of other functional groups including predators and detritivores. However, a longer survey period is needed to determine if the general patterns observed in the second season continue. The costs of these treatments should also be estimated for developers. In this study, cost of the compost product was $33.36 per 1000 ft2, plus cost of equipment and labor; however, retail value of compost would be higher, and cost varies by product. This research is part of a larger study to measure effects of soil mitigation after development to help reduce these inputs and help developed landscapes rebound. Ultimately, we will compare our arthropod population surveys with data being collecting from other University of Florida researchers measuring soil quality, hydrology, and turf health. Taken together, we will better understand how soil mitigation just prior to turfgrass and plant installation will affect long- term landscape establishment and ecosystem services.

Acknowledgements

This study would not have been possible without the collaboration and research interests of On Top of the World Communities (Ocala, Florida) particularly Philip Hisey, landscape superintendent. This project was also initiated and led by Dr. Eban Bean, whom we thank for the opportunity to collaborate. We also thank Rebecca Perry, Kendall Stacey, Alex LoCastro, and J.

Bryan Unruh for their assistance in field work and data collection. Lastly, we thank the Center for Landscape Conservation and Ecology, and UF IFAS Research for their continued collaboration and support.

Figure 2-1. Aerial view of study site showing the nine properties (lot 3-5, 7, 12-16), three outlined blocks, and three treatments within each block. Imagery, Fair use Attribution, Google, ©2020 Maxar Technologies, U.S. Geological Survey, Map data ©2020. Annotations by the author.

Figure 2-2. Lot during development, demonstrating typical site disturbance and soil compaction prior to plant installation. Photo courtesy of the author. April 18, 2018. Ocala, Florida, USA.

Figure 2-3. Example of backyard lawns at our study site, where each treatment was incorporated into the soil before plant installation on each lot. Photo courtesy of the author. October 18, 2018. Ocala, Florida, USA.

A A A

B AB B

A AB B

Figure 2-4. Overall arthropod abundance over the 2017-2018 survey period. Different letters adjacent to a sampling date indicate significant differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

A A B

AB B

A A AB AB B B

Figure 2-5. Overall arthropod richness at order level over the 2017-2018 survey period. Different letters adjacent to a sampling date indicate significant differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

A AB A A A B A AB AB

B B B

Figure 2-6. Combined decomposer abundance over the 2017-2018 survey period. Different letters adjacent to a sampling date indicate significant differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

Figure 2-7. Increasing levels of thatch decomposition as measured by mean % carbon lost through LOI analysis (±SEM).

Figure 2-8. Waxworm infection rate after exposure to soil samples for 9 days (mean ±SEM), collecting at three dates in the 2017 and 2018 seasons. According to Tukey-Kramer HSD means comparison (P < 0.05), significant differences between treatments exists (F82 = 3.55, p = 0.0311) between tillage (A) and till + compost (B) but not no-till (AB).

AB A

A A

Figure 2-9. Hunting billbug (Sphenophorus venatus vestitus) abundance over the 2017-2018 survey, collected by pitfall trapping (mean ±SEM). Different letters adjacent to a sampling date indicate significant differences between treatments using Tukey- Kramer HSD means comparison (P < 0.05).

A A A A A A A AB B

B B B B B B

Figure 2-10. Combined natural enemy abundance over the 2017-2018 survey, collected by pitfall trapping (mean ±SEM). Different letters adjacent to a sampling date indicate significant differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

Table 2-1. Results of ANOVA (alpha = 0.05) models to examine the effects of treatment, sampling date, the interaction of treatment and date. The effect of preexisting soil variability is incorporated as a blocked factor. Data Set Overall Model Treatment Date Treatment*Date df F Ratio Prob > F df F Ratio Prob > F df F Ratio Prob > F df F Ratio Prob > F Overall abundance F25,547 30.92 <0.0001 2 10.018 0.9277 7 40.503 <0.0001 14 2.3847 <0.0001 Order Level Richness F25,547 19.31 <0.0001 2 9.1404 0.0001 7 58.085 <0.0001 14 3.0803 0.0001 Decomposer Abundance F25,547 34.71 <0.0001 2 0.0184 0.9818 7 115.98 <0.0001 14 2.9622 0.0002 Predator Abundance F25,547 29.441 <0.0001 2 1.9443 0.1441 7 95.748 <0.0001 14 3.7246 <0.0001 Hunting Billbug Abundance F25,547 14.80 <0.0001 2 10.0181 <0.0001 7 40.5026 <0.0001 14 2.3847 0.0031 Thatch Decomposition F20,26 40.2621 <0.0001 2 1.1570 0.3394 2 196.2665 <0.0001 4 0.5376 0.7103 Waxworm Infection by EPN* F25,107 5.3575 <0.0001 2 3.5542 0.0331 10 19.9605 <0.0001 5 1.7460 0.0842 *For Waxworm infection levels, block was not significant factor; however, the effect of lawn type (front or back lawn) was slightly significant (F1 = 2.7691, p = 0.0999).

CHAPTER 3 NATIVE AND EDIBLE PLANTS ENHANCE ECOSYSTEM SERVICES THROUGH KEY PEST AVOIDANCE AND MULTIFUNCTIONALITY IN RESIDENTIAL LANDSCAPES

Abstract

Tea scale, Fiorinia theae, has long been one of the most important pests of Ilex and

Camellia plants, particularly in the southeastern United States. This exotic armored scale insect

(Hemiptera: Diaspididae) reduces host plant health and function, and often requires insecticide use, which pose risks to non-target organisms. While the use of Ilex and Camellia spp. as landscape ornamentals for aesthetic function is firmly established, we have a poor understanding of species-level susceptibility to F. theae. Additionally, two species, Ilex vomitoria and Camellia sinensis, are emerging tisane- and tea-producing commodities in the region, respectively. We propose that these multi-functional, consumable plants may be well-suited for residential landscapes where they may provide enhanced ecosystem services compared to some of their conventional ornamental congeners. However, the potential impact of key pests, like F. theae, on these species should be evaluated to anticipate pest pressure that may undermine or offset benefits. In this study, we examine six species within the known host range of tea scale, comparing non-native I. cornuta ‘Dwarf Burford’, C. japonica, C. sasanqua and C. sinensis, along with native I. opaca and I. vomitoria. We found that host species show a wide range of susceptibility to F. theae and associated damage, with the two native Ilex species and tea- producing C. sinensis displaying the greatest resilience. These results may help guide plant selection decisions to reduce the impact of a key pest and to integrate edible plants to diversify and enhance residential landscapes.

Introduction

In recent decades, urban landscapes have rapidly expanded (Brown and Vivas 2005) and become more relevant due to their far-reaching impacts and the novel interactions that occur within them (Raupp et al. 2010, Dale and Frank 2018). Growing evidence of large-scale urban homogenization demonstrates the increasingly important role of decisions regarding the creation and modification of urban plant communities, selecting plants based on various environmental, cultural, and aesthetic traits, each of which contribute to ecosystem services (McKinney 2006,

Groffman et al. 2014, Hall et al. 2016). On a basic level, proper plant selection and landscape design may be best exemplified by choosing plants based on their adaptability to local biotic and abiotic factors (Dale et al. 2016). However, beyond plant health and pest abundance, evaluation of the ecosystem services provided by individual plant species in urban ecosystems is often lacking (de Bello et al. 2010) and ecosystem disservices from residents’ perspectives, such as attracting undesirable urban animals or having an unconventional appearance, are often ignored

(Larson et al. 2019). Additionally, socioeconomic differences, environmental priorities, and geographic regions typically drive plant selection decisions in residential landscapes (Goddard et al. 2013, Avolio et al. 2018, Padullés Cubino et al. 2020). Padullés Cubino et al. (2020) suggest that managers and policy-makers should consider residents’ priorities for plant attributes in addition to plant availability and monetary costs. Further, we argue that alternative, underutilized species exist that fulfill consumer needs and may offer additional benefits to residents and the environment, particularly within the southeastern United States.

Camellia and Ilex are two widely used landscape ornamental plant genera in the southeastern U.S. that provide similar form and function. Camellia species (Ericales: Theaceae) are valued for their cool-season flowers on forms ranging from low shrubs to small understory trees. Camellia japonica L. and Camellia sasanqua Thunb. (or sasanqua types) are the most

commonly produced and planted Camellia species, each with numerous cultivars providing a range of bloom periods and floral traits. Ilex species (Aquifoliales: Aquifoliaceae) are also valued for their wide range of forms (e.g., hedges, columnar, weeping, tree-form) and winter aesthetic value, producing bright red berries against attractive dark green foliage. Numerous Ilex hybrids and cultivars are available, including native species such as the small tree American holly (Ilex opaca Ait) and nonnatives, such as Chinese holly (Ilex cornuta Lindl.), commonly used as hedges. Both genera are broadleaf evergreens, a category comprising the greatest portion of gross sales ($839 million in 2006) of all nursery crops, including $119 million in Florida

(USDA-NASS 2007). Despite this value, the services provided by these and other similar ornamental plants once installed are often reduced by herbivorous insect pests that frequently outbreak in urban landscapes (Braman et al. 1998, Raupp et al. 2010).

Most arthropod damage to ornamental plants is attributed to only a few herbivore groups, referred to as key pests (Raupp and Noland 1984, Raupp et al. 1992, Harris et al. 2004), who reduce the aesthetic and functional value of plants (Nielsen 1990b). Among the most ubiquitous and difficult to control key pests are sap-feeding insects, like scale insects and other Hemipterans

(Raupp et al. 2010, Zvereva et al. 2010). Scale insects reduce aesthetic quality (Frank et al.

2013), growth, and photosynthesis (Cockfield et al. 1987, Zvereva et al. 2010), and are among the most-targeted pests in urban landscapes with insecticides (IR-4 2007, Braman et al. 2015).

Armored scales (Hemiptera: Diaspididae) alone are estimated to cause over $2 billion in annual economic losses in the U.S. (Kosztarab 1990, Miller and Davidson 2005). One such key pest,

Fiorinia theae, has been established in North America for well over a century (Sasscer 1912) and is widely distributed in the southern half of the United States (Miller 2016). Like most armored scales, tea scale is polyphagous, with plant host records from at least 14 genera in 12 families

(García Morales et al. 2016). This insect is one of the ten most important scale insect pests in

Florida nurseries (Dekle 1965) and a serious global pest (Beardsley and Gonzalez 1975, Miller and Davidson 1990).

Within its host range, tea scale is most commonly found on Camellia and Ilex species

(Kuitert and Dekle 1972, Munir and Sailer 1985, Miller and Davidson 2005) and is known as the most destructive pest of Camellias in the southeastern U.S. (English and Turnipseed 1940,

Kouskolekas and Self 1973, Trehane 2007). Heavily infested Camellia leaves become chlorotic, may prematurely drop (English and Turnipseed 1940), and plants flower poorly and suffer twig dieback, resulting in plant death in some cases (Munir and Sailer 1985). In addition to direct feeding damage, armored scale infestations increase plant sensitivity to abiotic stress like drought (Cockfield and Potter 1986, Dale and Frank 2017). Among Ilex spp., Burford hollies

(e.g., I. cornuta ‘Burfordii’ and ‘Dwarf Burford’) are consistently associated with severe tea scale infestations (Kuitert and Dekle 1972, Gilman and Watson 1993, Hesselein et al. 1999). Tea scale, and other armored scale management is heavily reliant on insecticides, which have become safer and more effective in recent years, but can still pose non-target risks to beneficial organisms and the environment (Raupp et al. 2001, Rebek and Sadof 2009, Cloyd and Bethke

2011, Frank 2012, Godfray et al. 2015).

Among the most effective integrated pest management strategies in urban landscapes is proper plant selection for key pest avoidance (Raupp et al. 1992). Despite being well-established as the key pest of two prominent ornamental genera and the target of frequent, recurring insecticide applications, a species-level host comparison has not been performed. Previous studies only mention indications of variability in host susceptibility within these genera, ranging from some to no differences (Kouskolekas and Self 1973, Nagarkatti et al. 1979). Interestingly,

Ilex vomitoria Aiton and Camellia sinensis (L.) Kuntze are emerging specialty crops in the southeastern U.S., generating interest as consumable ornamental plants due to their caffeine- containing leaves. Camellia sinensis is the most economically important Camellia species globally, producing the second most-consumed beverages worldwide (Chang 2015). The growth habit, tolerance to sun and shade, tolerance to hedging, and 50-80 year longevity may make C. sinensis an attractive candidate for residential landscapes (Bezbaruah and Barbora 1983, Manivel

1998). Ilex vomitoria, best known as yaupon holly, is a second caffeinated tea-producing shrub species, but is native to the southeastern U.S. (USDA-NRCS 2019). Camellia sinensis and I. vomitoria are both documented tea scale hosts; however, reports lack quantitative measurements of susceptibility relative to congeners and observations suggest reduced pest pressure (Sasscer

1912, Howell and Ramona 1973, Nagarkatti et al. 1979, Galle 1997, Gilman and Watson 2014).

To make residential landscape plant selections that maximize value to humans and the environment, it is important to understand the relative ecosystem services and disservices associated with species of interest. Working towards this understanding, we evaluated the susceptibility of I. vomitoria and C. sinensis alongside their conventionally used ornamental congeners to tea scale. We first asked if ornamental and tea-producing congeners vary in susceptibility to tea scale infestation. Second, to further evaluate the effect of tea scale on its host plant after infestation, we quantified the damage caused by tea scale feeding. To accomplish this, we conducted evaluations to quantify host plant susceptibility to tea scale infestations and feeding injury, with the prediction that conventional ornamental Camellia and Ilex spp. would be more susceptible than their caffeinated congeners to tea scale, but that there would be a range of susceptibility among all species.

Materials and Methods

Study Organisms

All selected plants are widely commercially available and were purchased from local nurseries having received no systemic insecticide applications, but only contact spray treatments, including neem oil. We kept plants in screenhouses for the duration of the study in Gainesville,

FL, USA and all were maintained without insecticide exposure for three months prior to beginning the study. We obtained 18-20 each of the following species: female Ilex opaca, wild- type female Ilex vomitoria, female Ilex cornuta ‘Dwarf Burford’, Camellia sinensis var. sinensis,

Camellia sasanqua ‘Shishigashira’ and ‘Mine-no-yuki’, and Camellia japonica ‘Mathotiana

(Rubra)’. All species are documented tea scale hosts (Kuitert and Dekle 1972, García Morales et al. 2016), were comparable in size, and were mature enough for retail sale. We repotted C. sinensis and C. japonica so that all plants in the study were in 8.5-liter plastic nursery pots.

Although plants had no apparent tea scale infestations, several weeks prior to beginning the experiment all were treated horticultural oil (Sun Spray Ultrafine Oil®, rate 23ml/L) to ensure equal baseline infestation. Plants were also treated with a broad-spectrum fungicide

(chlorothalonil, Daconil®, rate 3ml/L) as needed to suppress foliar leaf spot diseases. Plants were irrigated as needed (by hand and drip) and received slow-release fertilizer (Osmocote® 18-

6-12 + micronutrients) in the spring (19 g) and the summer (9 g). All Camellias were kept under a 30% shade cloth structure and received a half-dose of elemental sulfur (Espoma Organic Soil

Acidifier) in the spring.

Tea Scale Inoculations

To evaluate the susceptibility of each plant species to tea scale, we inoculated all plants and compared the severity of infestations and damage on each over time. Unlike many other

scale insect species, tea scale does not produce ovisacs or colonize twigs that can be bound to a new host (Cockfield and Potter 1986, Frank 2012). Therefore, similar to Chiu and Kouskolekas

(1980), we collected live scale-infested leaves and fastened them to leaves on un-infested hosts using a fine pin. To avoid tea scale host-preference bias (Cooper and Oetting 1986), we performed cross-genera inoculations, infesting all Ilex spp. with scale-infested C. sasanqua and

C. japonica leaves and all Camellia spp. with scale-infested I. cornuta leaves. Each plant was inoculated with four infested leaves or leaf sections attached by a metal pin to a mature leaf within the canopy, with the scale-infested underside placed onto the top surface of an un-infested host’s leaf. We performed three separate inoculations in 2018 and 2019 – summer, early autumn, and late spring. All tea scale life stages were present during each inoculation. Several weeks after the first inoculation, a new generation of tea scale was observed on each host species, confirming successful inoculations (Figure 3-3). For the duration of the study, inoculated plants were grouped by species with each group separated by an un-infested buffer plant, all kept on raised benches. Camellia groups were kept under a 30% shade structure. We began collecting data one year after the first inoculation, corresponding to 5-6 female and 10-11 male generations (65 and

34 days per generation, respectively) in our region (Munir and Sailer 1985).

Host Susceptibility Evaluation

To compare the susceptibility of each Ilex and Camellia species to tea scale, we destructively sampled each plant, removing and counting all leaves with any life stage of tea scale present. Of the infested leaves, up to 25 were randomly selected and examined under a dissecting microscope. Since females are the reproductive individuals and their successful development and reproduction indicates host viability, we counted all individuals identifiable as female (as early as second instar nymphs) and recorded the number of mature females with eggs.

Next, we calculated the product of total infested leaves per plant and gravid females per infested leaf to estimate the total number of gravid females per plant and gauge the susceptibility of each species to tea scale (Dale et al. in review). We also identified any other scale insect species present on leaves.

Damage caused by armored scale insects varies depending on pest and host species involved, feeding site and host plant susceptibility (Kosztarab 1990). Therefore, to evaluate the effects of infestation on each plant, we also recorded symptoms of damage and prevalence on infested leaves. Visible symptoms of tea scale feeding on Camellia spp. is chlorotic mottling, while Ilex spp. tend to prematurely drop leaves associated with scale infestation. Mottling per infested leaf was recorded for all species based on presence or absence of chlorotic leaf tissue visible from the top of infested leaves. Leaf abscission was quantified for all Ilex spp. by collecting fallen leaves from pots and screenhouse flooring, then determining the percent of fallen leaves infested with tea scale. Data collection for tea scale infestation and damage took place over 12 weeks, progressing sequentially in groups of six plants (one of each species) so that all material could be examined fresh. Identification of tea scale from each infested host species was confirmed and vouchered by the scale insect taxonomist at the Florida Department of Agriculture, Division of Plant Industry, using Miller and Davidson (2005).

Statistical Analysis

We analyzed each measure of host plant susceptibility using one-way analysis of variance

(ANOVA) with means separation by Tukey’s HSD test (P < 0.05). Differences between genera were compared using two-sample t-tests, with alpha = 0.05. All data were analyzed using JMP

Pro 14 (SAS Institute Inc 2019) and figures were constructed using R software 3.6.1 (R Core

Team 2019) with package ggplot2 (Wickham 2016). Fiorinia theae count data were log(x+1)

transformed prior to analysis to increase the normality of residuals, with assumptions of normality examined using the Shapiro-Wilk W Test. Data were also blocked by 2-week data collection intervals to account for changes in tea scale infestations over the 12-week data collection period. Dead or dying plants (7 of 112) were excluded from all analyses, as well as one outlier (>4 SD from the mean) from the mottling damage analysis.

Results

Host Susceptibility

One year after initial inoculation, tea scale infestation levels ranged from 3 to 825 infested leaves per plant, with a mean (±SEM) of 107 ±12 (median of 61 leaves) (Table 3-1). As previously reported, we found all species to be viable tea scale hosts. However, species-level susceptibility ranged from highly resistant to highly susceptible (Figure 3-1). Based on average susceptibility, Camellia spp. supported significantly more tea scale than Ilex spp. (t101.18 = 8.94, p

< 0.001). Interestingly, the native species, I. vomitoria and I. opaca, had the fewest scale-infested leaves per plant and gravid females per leaf among all species, with scales showing little dispersal from inoculation sites. In stark contrast, I. cornuta ‘Dwarf Burford’ became highly infested over the duration of the study, which is consistent with previous reports (Kuitert and

Dekle 1972, Gilman and Watson 1993, Hesselein et al. 1999). Camellia sinensis and C. sasanqua each had moderate infestation levels, but importantly, both were less severely infested than C. japonica. Notably, both tea-producing species (I. vomitoria and C. sinensis) were the least susceptible hosts to tea scale infestation within their respective genera.

Host differences were most apparent when comparing the number of females and gravid females per infested leaf (Table 3-1). For example, C. japonica averaged nearly six times as many females and gravid females per leaf than C. sinensis, despite having similar leaf area.

While both female counts follow the same trend, a strong difference in the percentage of females that were gravid emerged between genera. On average, 27.18% (1.31) of females on Camellia spp. hosts were gravid, compared to 13.10% (1.67) on Ilex spp. (t97.13 = 6.63, p < 0.001).

Host Plant Damage

Chlorotic mottling was observed on all Camellia spp., with an average of 28.49  2.86% of tea scale infested Camellia leaves exhibiting damage. Symptoms were most apparent and severe on C. japonica and least apparent on C. sasanqua (Table 3-2). As expected, at the genus level, Ilex spp. averaged statistically less mottling damage on infested leaves compared to

Camellia spp. (t83.89 = 6.76, p < 0.001) with only 7.33 1.46% of infested leaves displaying mottling. Within all Ilex spp., mottling damage was not readily apparent without close individual leaf examination. While the severity of mottling per infested leaf was not evaluated, a comparison of damage extent can be estimated by multiplying the mean occurrence of mottling on infested leaves by the number of infested leaves per plant (Table 3-2, Figure 3-2).

In contrast to Camellia spp., the primary symptom of tea scale infestation on Ilex spp. was premature leaf abscission following a period of heat stress in late summer, which is consistent with previous observations of leaf abscission associated with armored scale feeding and drought stress (Cockfield and Potter 1986). This was most evident on I. cornuta ‘Dwarf

Burford’ where numerous green leaves abscised. By examining abscised leaves, we found that

88% of abscised leaves from I. cornuta ‘Dwarf Burford’ were infested with tea scale, compared to only 12% of I. opaca and 1% of I. vomitoria (Table 3-3). The high percentage of scale- infested leaves abscised from I. cornuta ‘Dwarf Burford’ suggests an effect of scale feeding. In contrast, I. vomitoria leaves collected from the ground were best explained by one plant that died

and dropped its foliage. The partial defoliation of I. cornuta ‘Dwarf Burford’ and loss of infested leaves also best explains the large variability observed in the mean number of infested leaves per plant and overall susceptibility metric (Figure 1).

Discussion

Providing evidence to guide ornamental plant selection and increase ecosystem services in residential landscapes is an increasingly relevant need as rapid urbanization progresses. This study demonstrates how informed plant selection can meet existing aesthetic functions, while reducing pests and associated management inputs and increasing plant health. More specifically, we show that both native Ilex species provide good resistance to tea scale compared with the more widely planted exotic shrub, I. cornuta ‘Dwarf Burford’. Furthermore, while all Camellia species became infested with tea scale at levels that may warrant intervention, infestations on C. sinensis and C. sasanqua were substantially less severe than on C. japonica, the most commonly planted species within the genus. Finally, I. vomitoria and C. sinensis, the only two consumable species evaluated, were the least susceptible species within their respective genera. Thus, in addition to reduced tea scale pressure, selecting these tea-producing plant species provides supplemental ecosystem services in residential landscapes for the people interacting with them.

At the landscape level, we often encourage adoption of greater plant species diversity, abundance, and structural complexity to increase resilience and arthropod biodiversity (Raupp,

Shrewsbury, et al. 2001, Shrewsbury and Raupp 2006, Raupp et al. 2010). Plant characteristics like provenance are important in determining ecosystem services, such as reduced pest damage

(Raupp et al. 1992, 2010, Herms 2002) or bottom-up provision for wildlife (Burghardt et al.

2010). Although native plants were the least susceptible to tea scale in this study, there is growing evidence that plant selection should also consider species-specific traits and ecosystem

services like floral resources, refugia for natural enemies, and benefits to wildlife, regardless of provenance (Parsons et al. 2020). For example, there is evidence demonstrating that female I. vomitoria offer greater benefits to frugivorous birds compared to I. cornuta (McPherson 1987,

1988). For many landowners, watching or attracting wildlife is a major priority, on par with recreation and entertainment value (Goddard et al. 2013). For example, Lepczyk et al (2004) found that over 50% of homeowners intentionally planted and maintained vegetation for birds, and 45-64% carried out other activities to support birds, such as feeding birds and providing bird houses. In addition to their importance for many bird species, the fruit of both I. vomitoria and I. opaca are sought after by a variety of mammals in urban areas (Coladonato 1991, Martin and

Mott 1997). Ilex vomitoria foliage is an important browse source for white-tailed deer (Goodrum and Reid 1958, Martin and Mott 1997) but is also highly tolerant of defoliation (Lay 1957).

Conversely, other ornamental Ilex spp., including I. opaca and I. cornuta, are much less preferred for deer browsing (Conover and Kania 1988). Based on available information, of the plants evaluated, I. vomitoria and I. opaca provide the greatest ecosystem services to wildlife.

An important factor that has received growing attention host plant origin, particularly in urban and residential landscapes (Burghardt and Tallamy 2013, Padovani et al. 2019, Parsons et al. 2020). In our study, the two least susceptible host plants are native to North America, while the four more susceptible species are exotic but native to the same regions as tea scale. Thus, the evolutionary history of the host and insect may be a factor in observed pest pressure preference for the exotic plant species evaluated (Farrell et al. 1992). Much focus in recent years has been given to the potential for native plants to support greater insect herbivory, particularly as an ecosystem service for higher trophic levels such as songbirds (Burghardt et al. 2010, Narango et al. 2017, 2018). Although our study also indicates that native plant species provide enhanced

services, we demonstrate this in the context of exotic herbivores and reduced damage from an exotic key pest.

When comparing the two tea-producing species, there are some key differences to consider from other forms of pest pressure. Chief among these is a foliar anthracnose disease

(Colletotrichum sp. complex) that may pose a challenge in the residential landscape (Orrock et al. 2019). Based on our observations, black citrus aphids, Toxoptera auranttii (Hemiptera:

Aphididae), may pose an additional pest challenge on the harvestable new growth. Ilex vomitoria has few other pests that are likely to require management in the landscape. Similar to our findings, in previous trials, I. vomitoria has consistently shown good resistance to several other common Ilex pests in the southeastern United States. In trials of 231 and 137 Ilex selections, I. vomitoria cultivars were amongst only five species resistant to Florida wax scale, Ceroplastes floridensis Comstock, and twolined spittlebug, Prosapia bicincta (Say) (Braman and Ruterj

1962, Hodges et al. 2001). In these studies, resistance benefits were less consistent for the other

Ilex sp. evaluated. I. opaca selections were highly susceptible to twolined spittlebug, while I. cornuta cultivars exhibited good resistance (Braman and Ruterj 1962). Conversely, I. opaca cultivars (with the exception of ‘Carolina No. 2’) exhibited resistance to Florida wax scale, while most I. cornuta cultivars were moderately to highly susceptible (Hodges et al. 2001).

We found significant variation among plant species in tea scale susceptibility. Although the underlying mechanisms determining scale insect susceptibility remain poorly understood and were outside the scope of this project, there are several potential factors to consider. Alongside temperature and rainfall, humidity is one of the primary climate conditions that influences armored scale life history (Beardsley and Gonzalez 1975). Tea scale prefers to settle and feed on the abaxial leaf surface where stomata are located, likely due to less exposure to predation and a

more stable microclimate with elevated humidity (Watson et al. 2015). Although we did not compare stomata between our species, sugarcane scale Gannaspis (=Melanaspis) glomerata

(Green) abundance has been positively correlated with host stomatal density (Agarwal and

Sharma 1961). Thus, differences in stomatal density among Ilex and Camellia species may contribute to our results and warrant investigation. A more common explanation for the general pest-resistant qualities of I. vomitoria is the caffeine content of twigs and foliage. This hypothesis has merit as caffeine and related methylxanthines have been implicated as endogenous pesticides that deter or even kill herbivores. However, given the evolutionary history of tea scale and its native host, C. sinensis, tea scale has likely evolved some level of caffeine tolerance (Nathanson 2013). In support of this, we found that tea scale infestations reached similar levels on the caffeine-containing foliage of C. sinensis and caffeine-lacking C. sasanqua.

Therefore, mechanisms other than caffeine content may be driving host susceptibility.

Standardizing environmental and cultural care allowed us to examine the effects and extent of tea scale infestation across several plant species with minimized unexplained variation.

Unfortunately, standardization may not always align with the best management practices for each host species involved. Symptoms associated with abiotic stress appeared most often on C. sasanqua, resulting in some loss of infested material prior to data collection. All plants in this study were commercially propagated as single-stem trunks except for C. sasanqua, where four rooted cuttings comprised each potted plant. Partial dieback of one or two stems in several pots could be a consequence of the smaller, individual root systems of the cuttings were less resilient to stress factors. Prior to initiating our tea scale infestations, we treated all plants with horticultural oil insure equally un-infested plants, but several other scale insect species were found during the course of the experiment. For example, a population of purple scale

(Lepidosaphes beckii Newman, 1869) developed on the I. cornuta ‘Dwarf Burford’ plants, eventually co-infesting some leaves along with tea scale. Additionally, aphids (Toxoptera auranttii Boyer de Fonscolombe) appeared on new growth of all Camellia spp., and southern red mite (Oligonychus ilicis MgGregor) became damaging enough on C. sasanqua and C. japonica to warrant the use of a selective miticide. Despite these supplemental infestations and interventions, tea scale was by far the most predominant herbivore, and our results represent similar interactions that may occur in a residential landscape, where multiple herbivore groups are interacting.

Another shortcoming is that while our damage metric appeared to proportionally reflect the aesthetic effects of tea scale feeding, it did not take into account the severity of mottling on individual leaves. Therefore, a large area of mottling on a Camellia spp. leaf and a small stripe of chlorosis on an Ilex sp. were both deemed “present”, but the latter damage may be undetectable during most landscape inspections. Furthermore, we also recorded many other organisms associated with the Camellia and Ilex spp. of interest. To date, we have found wax scale

(Hemiptera: Coccidae: Ceroplastes sp.) on stems of male I. vomitoria shrubs and Latania scale

(Hemiptera: Diaspididae: Hemiberlesia lantania) on the berries of female I. vomitoria, but none were found on the leaves. Aphids (Hemiptera: Aphididae: Toxoptera auranttii) were occasionally seen feeding on new growth of both I. vomitoria and C. sinensis, but disappeared without intervention from the former, while infestations on the latter required control. As mentioned, southern red mites (Acari: Tetranychidae, Oligonychus ilicis) were found in abundance on C. japonica and C. sasanqua, causing foliar stippling damage to both species; however, this damage was not observed on C. sinensis. Flatid planthoppers nymphs and adults

(Hemiptera: Flatidae, Metcalfa sp.) were observed on field-grown tea, but no damage was

visible. To our knowledge, we report the first observations of the following pests on tea in

Florida: white peach scale (Hemiptera: Diaspididae: Pseudaulacaspis pentagona), citrus mealybug (Hemiptera: Pseudococcidae: Plannococcus citri) and Florida wax scale (Hemiptera:

Coccidae: Ceroplastes floridensis). We also received a new county record (Alachua Co.) for a predatory thrips, Aleurodothrips fasciapennis, which was frequently observed on several infested host species.

Ultimately, plant selection decisions are based on a range of ecosystem services and disservices, as well as societal and aesthetic factors, and commercial availability (Avolio et al.

2018). However, in many cases, the extent of services and disservices associated with different species are unknown. Landscape managers and homeowners, when faced with a wide variety of planting options, will benefit from evidence-based information on the function and benefits of available plant options. While a single plant trait is unlikely to drive widespread adoption, this study offers important guidance for key pest avoidance, reduced insecticide use, incorporating native and edible plants into a landscape that offer a variety of ecosystem services. The residential integration of edible landscape plants does call for further research to identify pest control options and tactics that are compatible with plants intended for foliage harvesting and tea or tisane production. As urbanization continues, these seemingly minor decisions made by homeowners or landscape developers will have increasing influence on the organisms and functionality of urban ecosystems. Proper plant selection can promote sustainability without compromising aesthetic values and may introduced desirable new traits to the residential landscape.

Acknowledgements

We thank Lauren Dana, Mark Wilhelm, Jason Kuan, Jackson Jablonski, and Tanner

Felbinger for their assistance in data collection, inoculations, and plant care.

Table 3-1. Susceptibility of Ilex and Camellia species to Fiorinia theae, as measured by the number of infested leaves per plant, total and gravid females per infested leaf, and the susceptibility metric (means  SEM). Host Species N Infested leaves Females Gravid females Susceptibility (infested per plant per leaf per leaf leaves × gravid) Ilex vomitoria 19 25.37  4.72 b 1.82  0.31 d 0.31  0.13 d 5.10  1.24 c Ilex opaca 17 19.53  2.80 b 3.05  0.27 cd 0.38  0.12 d 7.24  2.36 c Ilex cornuta 16 168.50  52.76 a 5.93  1.92 bc 1.21  0.52 cd 601.84  425.55 b Camellia sinensis 18 136.17  25.35 a 5.69  0.88 bc 1.42  0.27 bc 197.18  54.19 b Camellia sasanqua 16 118.63  23.60 a 9.31  2.45 b 2.77  0.76 b 414.76  174.74 b Camellia japonica 19 178.11  19.00 a 31.07  4.31 a 8.50  1.39 a 1463.57  244.07 a

F F5,95.38 = 24.99 F5,96.23 = 39.85 F5,96.03 = 40.18 F5,99 = 38.6 P <0.0001 <0.0001 <0.0001 <0.0001 Different letters within a column indicate significant differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

Figure 3-1. Host susceptibility metric (mean  SEM) of Ilex and Camellia spp. shrubs to tea scale, Fiorinia theae. The susceptibility metric is the product of the number of infested leaves per plant and number of gravid females per infested leaf. Different letters indicate statistical differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

Table 3-2. Mottling damage observed on Ilex and Camellia species due to Fiorinia theae feeding, as measured by the number of infested leaves per plant, percentage of infested leaves with mottling, and their product as a damage metric (means  SEM). Host Species N Infested leaves % scale-infested Damage (infested leaves per plant leaves with mottling × % with mottling) Ilex vomitoria 19 25.37  4.72 b 11.10  2.80 c 3.92  1.30 c Ilex opaca 17 19.53  2.80 b 4.35  1.68 c 0.52  0.17 c Ilex cornuta 15 124.73  31.49 a 5.93  2.75 c 13.20  7.91 c Camellia sinensis 18 136.17  25.35 a 27.44  5.63 ab 39.41  9.32 ab Camellia sasanqua 16 118.63  23.60 a 15.50  2.50 bc 22.31  7.11 b Camellia japonica 19 178.11  19.00 a 40.42  4.17 a 76.73  11.96 a F F5,94.33 = 26.47 F5,93.7 = 17.88 F5,93.53 = 28.7 P <0.0001 <0.0001 <0.0001 Different letters within a column indicate statistical differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

Figure 3-2. Mottling damage metric (mean  SEM) of Ilex and Camellia spp. shrubs infested with tea scale, Fiorinia theae. Damage is the product of the number of infested leaves per plant and mean percent of leaves with visible mottling. Different letters indicate statistical differences between treatments using Tukey-Kramer HSD means comparison (P < 0.05).

Table 3-3. Number of leaves and percentage of leaves infested with Fiorinia theae, that prematurely abscised from Ilex spp. during an environmentally stressful period in late summer. Host Species N Abscised leaves % Abscised leaves with F. theae

Ilex vomitoria 1835 1% Ilex opaca 183 12% Ilex cornuta 2397 88% Abscised leaves are ca. 1/3 of the total collected.

Figure 3-3. Inoculation method demonstrating the pinned leaf used to inoculate new host plants. Photo courtesy of the author. September 20, 2018. Gainesville, Florida, USA.

CHAPTER 4 CONCLUSIONS

As urban areas expand in area and in interaction with a greater proportion of humanity and their effects become more far-reaching, it is imperative that we develop strategies to increase ecosystem services provided by urban plants. During the development process, urban landscapes undergo severe disturbance, often resulting in the partial or complete removal of the existing landscape, including flora, fauna, and topsoil. Ornamental trees, shrubs, and turfgrasses are installed in these disturbed sites and immediately predisposed to stresses associated with disturbance. In this thesis, we studied the effects of disturbed soil alongside soil mitigation treatments of tillage, and tillage combined with a compost that may reduce the effects of disturbance or benefit the populations of invertebrates that recolonize this areas, along with the ecosystem services they provide. We found that tillage alone showed no consistent benefits or disadvantages compared to untilled soils, but that the combination of tillage and compost showed some benefits compared to the untilled soils. The tillage + compost treatment increased invertebrate richness, and appeared to have some moderate benefits to detritivore, predator, and overall abundance, but only at select dates during the second season of sampling. Furthermore, tillage and compost treatment had no negative effect on the ecosystem services provided by detritivores for thatch decomposition. Conversely, the tillage and compost treatment was associated with decreased activity of entomopathogenic nematodes, which may have been a factor in more abundant hunting billbugs in the same plots. Overall, our results suggest that tillage alone did not show benefits for the reestablishing invertebrate lawn community, but tillage and compost showed some moderate benefits and a potential negative effect that requires further sampling to determine if patterns continue. However, if tillage and compost treatments are found to be beneficial for other aspects of landscape health, such as bulk density, nutrient retention, and

enhanced root growth, then our results add credence to this as a low-cost and simple way to reduce stresses imposed by disturbance on the plants and increase richness of the invertebrate communities occupying them.

The plants selected to occupy urban and residential landscapes also play a vital role in the ecosystem services that these spaces provide. To inform better shrub selection, we also examined woody ornamental plants from two widely used genera in the southeastern U. S., as well as two members of these genera less common to the landscape but which may offer additional benefits.

Specifically, we evaluated host susceptibility to a key pest, tea scale (Fiorinia theae). We learned that yaupon holly, Ilex vomitoria, and tea, Camellia sinensis, were the least susceptible members of their respective genera tested, supporting their use in the landscape by offering reduced tea scale susceptibility compared to some ornamental congeners, with additional benefit for humans and landscape interaction as edible, harvestable plants. Further, we found that both native plants tested, yaupon holly and American holly (Ilex opaca), were highly resistant to tea scale and offer the greatest ecosystem service benefits when considering their other values, such as excellent adaptability to stressful environments best seen in yaupon holly, and benefits to native birds and other wildlife compared to a non-native and more widely planted congener, Ilex cornuta ‘Dwarf

Burford’.

These studies investigated two aspects of creating and maintaining urban landscapes, with a focus on residential landscapes of the southeastern U.S. This information will be useful when planning urban development to mitigate the effects of soil disturbance and installing plants to guide selection towards species that offer greater ecosystem services and enhance the sustainability of residential landscapes.

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BIOGRAPHICAL SKETCH

Matthew Borden spent most of his early years in eastern Zimbabwe and Cape Town,

South Africa, where he developed a keen appreciation of the natural sciences, particularly in plant health, insects, and their interactions. He returned to the United States to attend Virginia

Polytechnic Institute and State University, graduating Cum Laude in 2015 with his bachelor’s degree in Biological Sciences, minoring in entomology and horticulture. After spending a year in plant pathology work and IPM plan development, Matthew moved to the University of Florida to pursue his Master of Science degree in entomology and nematology with Dr. Adam Dale, as well as the Doctor of Plant Medicine degree, an interdisciplinary program exploring many aspects of plant health management and diagnostics. For his thesis, he studied the effects of soil mitigation strategies on invertebrates that dwell in residential lawns, with the goal of proactively improving landscape resilience. He also took on a second project examining differences of infestation levels and damage of tea scale, Fiorinia theae, to six species of Ilex and Camellia spp. shrubs. Both projects were designed to inform ways of making urban landscapes more sustainable. Matthew would like to use his knowledge and experienced gained at the University of Florida to work in pest management plan development and searching for ways to make human interaction with natural resources and landscapes more sustainable.