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ABSTRACT

LONG, LAWRENCE CHARLES. Effects of Urbanization and Warming on Trees, Pests, and Urban Birds (Under the direction of Dr. Steven D. Frank).

Urbanization is converting forests into small pockets of trees and shrubs interspersed among human-dominated landscapes. Urban forests often consist of both planted trees in

managed landscapes and unmanaged urban forest fragments. Some tree pests are more abundant on urban trees because they benefit from higher temperatures associated with the urban heat island effect, and some natural enemies, especially birds, are less abundant due to habitat loss associated with urbanization. The broad purpose of this work is to investigate the effect of urbanization and warming on pest density, tree growth, predation services, herbivory, and urban bird community composition.

Scale insects are ubiquitous pests of urban trees in the southeastern United States. Their fecundity and survival on planted ornamental trees increases by orders of magnitude across just a few degrees of warming. I wondered if urban forest fragments could buffer the effects of

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mid-latitude climate which would simulate future warming. Quercus phellos of northern origin grew more than trees of local origin and Parthenolecanium quercifex, another common scale insect, of northern origin attained greater density than scales from local origin. However, trees infested with northern scales grew less regardless of their origin, suggesting that any benefit to tree growth due to climate warming could be counteracted by benefits to pests.

Theory predicts that complex habitats support more natural enemies, which exert top-down control over arthropods. Forest fragments are the most complex habitat in urban environments and as such could support greater predator activity than simpler habitats.

Therefore, foliavores could be more abundant on trees growing in simpler managed habitats such as ornamental landscapes and downtown areas and those trees would suffer greater herbivory than forest trees. I found that bird, but not arthropod predation was greater on trees growing in urban forest fragments. Foliavores were more abundant and herbivory greater on trees in urban forest fragments than managed landscapes. I suggest that urban forest fragments support greater basal resources for foliavores and other arthropod prey, thereby mediating top-down effects of birds on herbivory.

Birds are particularly sensitive to urbanization. For example, loss of nesting and foraging sites and decreased arthropod availability due to prevalence of non-native landscaping have been

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Effects of Urbanization and Warming on Trees, Pests, and Urban Birds

by

Lawrence Charles Long

A dissertation submitted to the Graduate Faculty of North Carolina State University

in partial fulfillment of the requirements for the degree of

Doctor of Philosophy

Entomology

Raleigh, North Carolina 2019

APPROVED BY:

_______________________________ _______________________________ Dr. Steven D. Frank Dr. Barbara Fair

Committee Chair

_______________________________ _______________________________ Dr. Michael Reiskind Dr. Robert Dunn

_______________________________ Dr. Vincent D’Amico

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ii

BIOGRAPHY

Lawrence Long was born and raised in Middletown, Ohio. He spent much of his time outside, feeding an early addiction to the natural world. When he wasn’t outside his nose was in a field guide or textbook looking up what little flora and fauna his neighborhood had to offer. Just as often though, he was reading those books to learn about plants and animals he had never seen so that he could be ready if he ever encountered them. Lawrence graduated with a degree in zoology and minor in entomology from The Ohio State University in 2009. He subsequently began graduate studies at Ohio State under the direction of Dr. Daniel Herms, earning his M.S. in entomology in 2013. Lawrence was hired to be the naturalist and director of education at

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ACKNOWLEDGMENTS

I thank Steve Frank first and foremost for his expert guidance and support. I also thank my committee members Barbara Fair, Michael Reiskind, Rob Dunn, and Vince D’Amico for the unique perspective and invaluable feedback that each brought to my research. I also thank my fellow Frank Lab graduate students: Adam Dale, Emily Meineke, Kristi Backe, Sarah Parsons, Christina Mitchell, Ian McAreavy, Caleb Wilson, April Hamblin, Amanda Anderson, and

Samantha Larson for their camaraderie and insight. Thanks to all the student workers who helped with data collection and to Matt Bertone for help with specimen identification. Thanks to

Annemarie Nagel for adeptly managing grad student requests for vehicles, equipment,

technicians, and her time. Thanks to Frank Lab post-docs, Michael Just and Nora Lahr, as well as Elsa Youngsteadt, who provided much advice and discussion without which would have made my time at NCSU that much more challenging. I thank my friends and family for providing me the inspiration (positive or negative) to stay motivated. Last but not least, I thank my wife Deanna, who has been supportive of me throughout this endeavor and whose patience, love, and encouragement has kept me focused.

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iv

TABLE OF CONTENTS

LIST OF TABLES ... vi

LIST OF FIGURES ... vii

Chapter 1: Urban forest fragments buffer trees from warming and pests ... 1

Abstract ... 2

Introduction ... 3

Methods... 6

Temperature, water stress, M. tenebricosa density, and natural enemy variation ... 6

Separating the effects of temperature from other environmental factors affecting M. tenebricosa ... 9

Effect of background temperature on M. tenebricosa abundance ... 11

Results ... 12

Temperature, water stress, M. tenebricosa density, and natural enemy variation ... 12

Separating the effects of temperature from other environmental factors affecting M. tenebricosa ... 13

Effect of background temperature on M. tenebricosa abundance ... 13

Discussion ... 14

Conclusions ... 18

References ... 21

Chapter 2: Pests reduce benefits of warming for northern trees ... 34

Abstract ... 34

Introduction ... 35

Methods... 38

Results ... 41

Local and Latitudinal Effects of Temperature on P. quercifex ... 41

Parthenolecanium quercifex Density ... 42

Quercus phellos Growth ... 43

Discussion ... 43

References ... 48

Chapter 3: Urban forest fragments host greater bird predation, herbivore abundance, and herbivory compared to managed ornamental landscapes ... 60

Abstract ... 60

Introduction ... 61

Methods... 64

Study Design ... 64

Predation Rate ... 64

Chewing Foliavore Abundance and Richness ... 67

Herbivory ... 67

Results ... 68

Predation Rate ... 68

Chewing Foliavore Abundance and Richness ... 69

Herbivory ... 69

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v

References ... 75

Chapter 4: Effects of urban habitat on bird communities, arthropod abundance, and bird foraging ... 90

Abstract ... 90

Introduction ... 91

Methods... 94

Study Design ... 94

Characterization of bird community ... 96

Arthropod Abundance ... 97

Predation Rate ... 98

Results ... 99

Characterization of bird community ... 99

Arthropod Abundance ... 101

Predation Rate ... 102

Discussion ... 102

References ... 106

APPENDICES ... 121

Appendix A: Supplemental Material for Chapter 3 ... 122

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vi

LIST OF TABLES

Table 2.1 Effects on Parthenolecanium quercifex nymph density. Effects are significant at the a<0.05 if listed in orange. Effects listed in red are significant at a<0.01. ... 55 Table 2.2 Effects on gravid Parthenolecanium quercifex density. Effects are significant

at the a<0.05 if listed in orange. Effects listed in red are significant at a<0.01. ... 55 Table 2.3 Effects on Quercus phellos growth. Effects are significant at the a<0.05 if

listed in orange. Effects listed in red are significant at a<0.01. ... 55 Table 3.1 The percent of total attacks by birds or arthropods among the studied urban

tree habitats from each season. ...86 Table 4.1 Summary statistics for multiple response permutation procedure of bird

community and urban habitat type. Multiple comparisons made using

Sorensen distances with MRPP. ...113 Table 4.2 Indicator species analyses. All birds were significant indicators (p<0.05) for

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vii

LIST OF FIGURES

Figure 1.1 The effects of tree location on canopy temperature and water potential are illustrated using boxplots to demonstrate the range of values obtained. The median of the data range is marked by the line which divides each box. Boxes represent the interquartile range and upper and lower whiskers represent data outside the middle 50% of observations. Asterisks indicate significant

differences from Tukey HSD tests. (a) The average canopy temperature of urban landscape trees (n=16) was significantly greater than it was for trees growing at urban forest fragment edge (n=16) or interior (n=16). (b) The average predawn water potential did not differ among urban landscape (n=16), urban forest fragment edge (n=16) or interior trees (n=16). ... 29 Figure 1.2 The effect of tree location on mean Melanaspis tenebricosa density. (a) In

December 2016, planted landscape trees (n=17) had three orders of magnitude more M. tenebricosa than fragment edge (n=17) or fragment interior (n=17) trees in Raleigh, NC. (b) There was no difference in M. tenebricosa density among planted landscape (n=24), fragment edge (n=23), and fragment interior (n=24) trees in the Newark-Philadelphia urban area during November 2016. Asterisks indicate significant differences (P < 0.05) derived from post-hoc Steel-Dwass all pairs test. Error bars represent ± 1 standard error of the mean. ... 30 Figure 1.3 Effect of tree position on parasitoid wasp abundance. The total number of

parasitoid hymenopterans captured on sticky cards from three families

(Aphelinidae, Encyrtidae, and Signophoridae) were more numerous in landscape trees (n=13) than either forest fragment edge (n=12) or interior trees (n=11). Post hoc nonparametric multiple comparisons from Steel-Dwass all pairs test. Asterisks indicate significant differences (P < 0.05). Error bars represent ± 1

standard error of the mean. ... 31 Figure 1.4 Effect of tree position on Melanaspis tenebricosa density. Potted saplings that

were paired with landscape trees (n=14) had higher densities of M. tenebricosa than potted saplings paired with forest fragment edge (n=16) or interior trees (n=16). Asterisks indicate significant differences from Tukey HSD tests (P < 0.05). Error bars represent ± 1 standard error of the mean. Two of the potted saplings that were paired with urban landscape trees were destroyed by vandals during deployment. ...32 Figure 1.5 Effects of tree location on Melanaspis tenebricosa density by city.

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viii (n=17), forest fragment interior (n=17). New-Phil abbreviates the

Newark-Philadelphia urban area: landscape (n=24), forest fragment edge (n=23),

forest fragment interior (n=24). ...33 Figure 2.1 Boxplots showing the density of P. quercifex in warm urban landscapes and

cool urban forest fragments in Raleigh, NC and Newark, DE USA. Lowercase letters above boxplots represent pairwise differences from Dunn method (p<0.05). Trees growing in Raleigh Urban sites had 0.07 ± 0.02 (SEM) P. quercifex/cm, Raleigh Forests had 0.008 ± 0.003 P. quercifex/cm, Newark Urban trees had 0.01 ± 0.006, and no P. quercifex were detected in Newark

Forests. ...56 Figure 2.2 Boxplots displaying the average daily temperature (1981-2010) from weather

stations nearest the site of the common garden and locations from which P. quercifex and Q. phellos were sourced. Lowercase letters inside the boxplots represent pairwise differences from Tukey’s HSD (p<0.05). ...57 Figure 2.3 Density of (A) nymph and (B) gravid adult P. quercifex in the common garden

experiment. Lowercase letters inside boxplots indicate significant differences from Tukey’s HSD of main effect of P. quercifex origin (a<0.05). Detailed

statistics are available in Table 1 and Table 2. ...58 Figure 2.4 Tree diameter growth was affected by both Q. phellos origin and P. quercifex

origin. See table 3 for detailed statistics. ...59 Figure 3.1 Photos showing A) typical deployment of plasticine larva model, B) example

of bird predation, C) ant predation, and D) wasp predation. ...86 Figure 3.2 All pairwise differences in average bird and arthropod predation rate among

urban tree habitats from Tukey’s HSD for summer 2017 (A) and spring 2018

(B). Bars not sharing a letter indicate significant differences (a<0.05). ...87 Figure 3.3 Pairwise differences in average leaf-chewing herbivore abundance among

urban habitat types from Steel-Dwass method for summer 2017 (A) and spring 2018 (B). Bars not sharing a letter indicate significant differences

(a<0.05). ...88 Figure 3.4 Pairwise differences in average leaf area consumed (cm2) among urban habitat

types from Tukey’s HSD for summer 2017 (A) and spring 2018 (B). Bars not

sharing a letter indicate significant differences (a<0.05). ...89 Figure 4.1 Photos showing A) typical deployment of plasticine larva models and

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ix Figure 4.2 The proportion of vegetation coverage within a 50-meter radius of Q. phellos

growing among different urban habitats (urban forest fragments, residential and downtown areas). Lowercase letters above boxplots indicate significant

pairwise comparisons from Tukey’s HSD test (P<0.05). ...115 Figure 4.3 The (A) abundance, (B) species richness, (C) Simpson’s diversity, and

(D) Berger-Parker dominance of birds in urban forest fragments (Forest), residential neighborhoods (residential), and highly urban (downtown) areas. Different lowercase letters above boxplots indicate significant (P < 0.05)

pairwise differences among urban habitats. ...116 Figure 4.4 The (A) abundance, (B) richness, and (C) Simpson’s diversity of insectivorous

(blue bars), omnivorous (red bars), and granivorous (green bars) feeding guilds among urban forest fragments (Forest), residential neighborhoods (Residential), and highly urban (Downtown) areas. Different lowercase letters above the bars indicate significant (P<0.05) pairwise differences among site categories for each feeding guild. ...117 Figure 4.5 Nonmetric multidimensional scaling (NMDS) of bird community data in forest

(green), residential (blue), and downtown (red) urban habitats. The NMDS converged to a three-dimensional ordination after 119 iterations from an initial stress of 34.69 to a final stress of 15.89. ...118 Figure 4.6 The abundance of arthropods likely to be consumed by birds on Q. phellos

growing among different urban habitat types (urban forest fragments, residential areas and downtown). Lowercase letters above boxplots indicate significant

pairwise comparisons from Tukey’s HSD test (P<0.05). ...119 Figure 4.7 The total number of attacks by birds on plasticine model caterpillars deployed in

Q. phellos among different urban habitat types (urban forest fragments, residential areas and downtown). Lowercase letters above boxplots indicate significant

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1

CHAPTER 1: Urban forest fragments buffer trees from warming and pests

This chapter published in the March 2019 issue of the journal Science of the Total Environment

Long, L.C., D’Amico, V. & Frank, S.D. (2019) Urban forest fragments buffer trees from warming and pests. Science of The Total Environment, 658, 1523–1530.

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Abstract

Trees are important components of urban landscapes because of the ecosystem services they provide. However, the effects of urbanization, particularly high temperatures, can benefit chronic insect pests and threaten ecosystem services offered by urban trees. Urban forest fragments are an often-overlooked component of the greater urban forest which may help to mitigate the damaging effects of urbanization. Melanaspis tenebricosa (gloomy scale) is a

common pest of Acer rubrum (red maple) that becomes more abundant because of the urban heat island effect. We conducted observational and manipulative field experiments to test the

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3

Introduction

Urban forests provide many ecosystem services important for maintaining environmental health and human well-being (Mullaney et al., 2015a). However, urban trees are often under abiotic stress and have severe pest infestations (Frankie and Ehler, 1978; Raupp et al., 2010) that can reduce ecosystem services (Meineke et al., 2016). So, it is important to understand how stressors associated with urban environments and warming climate will affect urban trees. The urban heat island effect is caused by impervious surfaces that absorb solar radiation and emit heat, thus intensifying temperatures in cities (Oke, 1973; Oke et al., 1989; Taha, 1997) and contributing to tree stress (Cregg and Dix, 2001). Impervious surfaces also increase tree stress by reducing soil moisture (Savi et al., 2015) and increasing vapor pressure deficit which reduces photosynthetic water use efficiency (Oke et al., 1989; Lahr et al., 2018a). The urban heat island effect can benefit arthropod pests directly by increasing survival, fecundity, or rate of

development (Hart et al., 1986; Cregg and Dix, 2001; Sperry et al., 2001; Meineke et al., 2013; Dale and Frank, 2014a), or indirectly by increasing host plant stress and quality for pests (Hanks and Denno, 1993; Hanks et al., 1999; Huberty and Denno, 2004), or reducing top-down control by natural enemies (Meineke et al., 2014).

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4 coverage in a large city in the Midwestern U.S. (Nowak, 1994). This is a substantial contribution given that the same study found that trees covered only 11% of the total urban land area (Nowak, 1994).

Trees growing in urban forest fragments may also be cooler because they are not surrounded by impervious surface. The formation of ‘cool islands’ by forest fragments within large urban areas are evidence for this (O'Brien et al., 2012; Chen et al., 2014). Thus, trees in urban forest fragments may be buffered from heat-related stress and pest infestations.

Understanding if trees in urban forest fragments have fewer pests than landscape trees and untangling the mechanisms which contribute to differences in pest abundance will inform management of trees in both situations.

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5 more fecund on hot and dry A. rubrum than cool trees that received frequent supplemental water (Dale and Frank, 2017) suggesting an additive effect of drought and temperature. As such, heat is a primary factor affecting the abundance of M. tenebricosa and other scale insects on urban and rural trees but drought may also play a role (Meineke et al., 2013; Dale and Frank, 2014a, Dale and Frank, 2014b; Youngsteadt et al., 2014; Meineke and Frank, 2018).

Scale insects are ideal organisms for studying temperature effects on arthropod populations because they are sessile and cannot leave a host plant under stressful conditions. Thus, they are subject to the total complement of abiotic and biotic factors affecting them and the host on which they live. If trees in urban forest fragments are buffered from the urban heat island effect and other stressors associated with urbanization such as reduced water availability and soil compaction (O'Brien et al., 2012; Chang and Li, 2014; Mullaney et al., 2015a, Mullaney et al., 2015b; Song et al., 2015) it follows that they should have fewer M. tenebricosa, greater

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6 manipulative experiment to isolate the effects of temperature from soil and other environmental conditions by measuring the change in M. tenebricosa density on potted A. rubrum saplings placed in the same urban landscapes and forest fragments. Third, to further test the hypothesis that M. tenebricosa increases with temperature, we compared M. tenebricosa density in landscapes and forest fragments of a mid-latitude city to those of a cooler urban area that lies 3.95 degrees of latitude higher. Latitude, a major predictor of background climate, coupled with urban heat island effect are the main factors which contribute to the temperature of an urban area. Again, we predicted that landscape trees would have more M. tenebricosa than urban forest fragment trees. By comparing urban areas from differing background climates, we also create a scenario analogous to future climate change whereby conditions in the mid-latitude city could predict future pest abundance in the high-latitude urban area. We also predicted that A. rubrum in the mid-latitude city, would have more M. tenebricosa overall than trees in the cooler, higher-latitude urban area. Urban trees are an important part of the landscape in most cities (Nowak et al., 2001). It is critical to understand how urban forest fragments, a major component of the urban forest, buffer trees and their services from urban heat and warming global climate.

Materials and Methods

Temperature, water stress, M. tenebricosa density, and natural enemy variation:

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7 fragments were in highly urbanized areas. Specifically, we define urban forest fragments as any space within an urban area which contains trees >5.0 cm in diameter at breast height, and is not being actively managed (e.g. cultivation, mowing, or raking of the understory or pruning of the trees themselves). All landscape trees were planted within 50 m of an urban forest fragment. Fragment edge trees were rooted within 2.5 m of a forest edge and their crown extended outside of the continuous forest canopy. We included fragment edge trees in our design as an

intermediate location because trees growing there may be subject to some of the same stressors as trees planted in landscapes, but they may also be buffered from urban stressors because of their proximity to the forest fragment. Fragment interior trees were rooted >2.5 m inside the forest edge and their crowns were surrounded by other tree crowns. Study trees were distributed across 0.04 degrees latitude and 0.05 degrees longitude (from 35°48′10.22″N, 78°43′6.61″W to 35°45′36.00″N, 78°39′50.17″W). Urban forest fragments ranged in area from 0.18 ha to 12.13 ha with an average area of 2.17 ha (±0.74 ha).

To determine how tree location affects canopy temperature, we recorded temperature at 4-hour intervals from May 26, 2016 to September 26, 2016 with Thermochron iButton data loggers DS1921G (Dallas Semiconductor, Dallas, TX). To avoid inflated temperature readings caused by exposure to direct sunlight, the data loggers were positioned in the lower canopy of a subset (n = 16 per location) of our study trees. Temperature readings were averaged across the 123 active days to obtain the mean temperature of each tree and analyzed with ANOVA

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8 We measured pre-dawn xylem water potential to assess tree water stress using a

Scholander type pressure chamber (PMS Instrument Company, Albany, OR). In the same subset of study trees used to measure temperature, we pruned two 15 cm twigs with leaves intact from opposite sides of each tree canopy on the morning of August 12, 2016. Within 5 min of being abscised, the twigs were placed one at a time into the pressure chamber for measurement. Upon gradual pressurization of the twig we recorded the value at which water was released from the xylem and the mean of the two twig measurements per tree was taken to obtain an average water potential per tree. ANOVA was used to test for differences in water potential among landscape, fragment edge, and fragment interior trees where average tree water potential was specified the response variable and tree location the predictor.

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9 We compared abundance of parasitoids from three families previously shown to

parasitize M. tenebricosa (Dale and Frank, 2014b), among landscape, fragment edge, and fragment interior trees by hanging 7.6 × 12.7 cm yellow sticky cards (Olson Products, Medina, OH, USA) in the lower canopy of the subset of our study trees. Some sticky cards went missing and thus could not be used in the analysis. Sticky cards that were visibly damaged or tampered with were also removed from the analysis. Sticky cards were exchanged every 2 weeks while M. tenebricosa parasitoids were active from May 18 to June 7, 2016. We tested for overall

parasitoid abundance among tree locations using a Kruskal-Wallis test where the total number of parasitoids captured per tree was specified as the response variable and tree location the predictor variable. We used the Steel-Dwass method for post-hoc comparison of parasitoid abundance among locations (a = 0.05).

Separating the effects of temperature from other environmental factors affecting M. tenebricosa: To control for effects of soil conditions (e.g., type, nutrition, compaction, moisture) that may differ between landscapes, forest fragment edges, and interiors, we measured M.

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10 were moved to a nursery pad and watered with drip irrigation for two growing seasons which also permitted two generations for M. tenebricosa populations to build. On May 18, 2016, more composted bark mulch was added to the surface of each pot and water retaining polymer gel crystals (BioPlex Organics Plant Survival Solutions, Joy, PA, USA) were mixed with the medium according to label specifications for potted containers.

All M. tenebricosa within a 30 cm section of stem beginning 10 cm above the potting medium, on each sapling were counted using an Optivisor, DA-4/LX-4 (Donegan Optical Company, Lenexa, KS, USA). Potted saplings were deployed in the field by staking the pots within 1 m of the trunks of 16 trees per location (N = 48). Scale-free saplings (N = 24) were paired with half of the infested saplings to measure the number of M. tenebricosa scales that colonized potted saplings by raining down from the mature tree. The scale-free saplings underwent the same treatment as infested saplings but were stripped of all M. tenebricosa by visual inspection and hand removal prior to placement in the field. Once deployed the saplings each received 7.5 l of water twice per week which was sufficient to keep the water retaining polymer gel crystals hydrated at all locations. Melanaspis tenebricosa were counted again on the same 30 cm section of stem after 15 weeks in the field on September 9, 2016. The final M. tenebricosa density was log transformed and we used ANCOVA to determine how sapling location affected final M. tenebricosa density. We specified final M. tenebricosa density as the response variable and location as the fixed predictor. Initial M. tenebricosa density was specified as a covariate to determine if the final density of M. tenebricosa among tree locations was

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11 colonization of scale-free potted saplings varied among locations where final density of M. tenebricosa is the response and tree location is the fixed predictor. Tukey's HSD was used for post-hoc comparison of group means when significant differences were found among tree locations for any of the analyses in this experiment.

Effect of background temperature on M. tenebricosa abundance:

To determine the effect of background temperature on M. tenebricosa, we compared scale abundance for trees from Raleigh, North Carolina USA to trees from Newark, Delaware and Philadelphia, Pennsylvania USA. By comparing M. tenebricosa abundance across fragment interior, edge, and landscape trees at a higher latitude we mimicked the Raleigh experiment in which we examined M. tenebricosa density across the gradient of urban tree locations. Newark-Philadelphia study trees were distributed across 0.48 degrees of latitude (from 39°36′40.28”N, 75°43′19.85″W to 40°05′23.07″N, 74°59′09.62″W) and 0.61 degrees of longitude (from 39°40′32.14″N, 75°46′49.74″W to 40°05′23.07″N, 74°59′09.62″W). Sites in Newark, DE and Philadelphia, PA were part of the University of Delaware's FRAME program (Forest Fragments in Managed Ecosystems; https://sites.udel.edu/frame; (Handley et al., 2015)) and because of the similarity of latitude, longitude, and average annual temperature will henceforth be referenced as a single urban area called Newark-Philadelphia.

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12 generalized linear model. We specified M. tenebricosa density as the response and tree location, city, and their interaction as predictors. By including the interaction between city and tree location we were able to determine if M. tenebricosa responded differently to tree location in each urban area. Because M. tenebricosa density was over-dispersed we elected to fit it to a negative binomial distribution (White and Bennetts, 1996; Lindén and Mäntyniemi, 2011).

Results

Temperature, water stress, M. tenebricosa density, and natural enemy variation:

The mean temperature across all trees ranged from 24.4 °C to 27.2 °C. Mean temperature of planted landscape trees was greater than fragment edge trees by 1.2 °C and greater than fragment interior trees by 1.3 °C (P < 0.001, F2,45 = 58.44) (Fig. 1). Pre-dawn water potential ranged from −0.4 to −1.2 MPa with mean of −0.6 MPa but did not differ among planted landscape, fragment edge, or fragment interior trees (P = 0.27, F2,45 = 1.32) (Fig. 1).

Melanaspis tenebricosa density across all trees in Raleigh, NC in January 2016 ranged from 0 to 18.5 scales/cm. Its density was greater (P < 0.001, X2 = 46.53) by three orders of

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13 landscape trees than either fragment edge, or fragment interior trees (P < 0.001, X2 = 13.59; Fig. 3).

Separating the effects of temperature from other environmental factors affecting M. tenebricosa: Final M. tenebricosa density was greater on saplings paired with landscape trees than saplings paired with either fragment edge or fragment interior trees (P = 0.005, F2,40 = 6.17) (Fig. 4). As expected, initial M. tenebricosa density had a significant effect on final M. tenebricosa density (P < 0.001, F1,40 = 22.06). However, there was no significant interaction between sapling position and initial M. tenebricosa density (P = 0.204, F2,40 = 1.65). Cultivar had no significant impact on the initial (P = 0.70, F2,43 = 0.36) and final density (P = 0.71, F2,43 = 0.35) of M. tenebricosa. Colonization of initially uninfested saplings was low (0.3 ± 0.1 SEM M.

tenebricosa/cm) and did not differ among trees in landscape, edge, or interior locations (P = 0.27, F2,21 = 1.39) suggesting that colonization of potted saplings due to dispersal of first-instar M. tenebricosa from landscape and fragment trees was negligible during the time saplings were deployed.

Effect of background temperature on M. tenebricosa abundance:

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14 significant interaction between tree “location” and “city” which suggests that M. tenebricosa responded differently to tree location (landscape, fragment edge, fragment interior) in each city (Wald X2 = 16.28, P < 0.001) (Fig. 5).

Discussion

Understanding how tree pests respond to warming in different parts of the urban forest is vital to protecting the ecosystem services offered by trees as cities expand and the climate warms. Urban trees in managed landscapes such as residential neighborhoods, industrial areas, and business complexes are subject to infestation by pests that are less common in rural forests (Metcalf, 1922; Raupp et al., 2010; Youngsteadt et al., 2014). Higher urban temperatures result in greater survival and fecundity and are often the mechanism for this disparity (Meineke et al., 2013; Dale and Frank, 2014a, Dale and Frank, 2017). As such, scale insects and other urban tree pests may be indicators of changing climate and studies of their response to the urban heat island effect are valuable for predicting future threats to urban and rural trees (Youngsteadt et al., 2017; Lahr et al., 2018b). Because trees in urban forest fragments and landscapes are subject to the urban heat island effect and many of the same biotic and abiotic factors (Hanks and Denno, 1993; Tooker and Hanks, 2000) one may not expect to find differences in temperature or pest abundance. However, we show that A. rubrum trees growing in urban forest fragments are on average 1.3 °C cooler and have three orders of magnitude fewer M. tenebricosa than trees growing in managed landscapes of a mid-latitude city in the southeastern USA.

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15 stress. Moreover, we found greater overall density of M. tenebricosa in the warmer climate of our mid-latitude city, compared with the cooler climate of the higher latitude city. Ours is the first study to demonstrate that urban forest fragments mitigate the urban heat island effect on trees and thereby reduce tree pest abundance in a warm, mid-latitude city.

The urban heat island effect causes drought stress in urban trees by reducing soil moisture and increasing vapor pressure deficit (Cregg and Dix, 2001). Drought stressed plants require greater negative pressure to draw water from the roots through their xylem (Scholander et al., 1965). We did not find a difference in pre-dawn water potential among landscape and forest fragment trees which suggests that drought stress did not contribute to the differences in M. tenebricosa densities that we observed. Moreover, the water potential values we observed did not reach levels known to cause physiological impairment in woody angiosperms (Urli et al., 2013; Yin and Bauerle, 2017) thus, the trees were not suffering from chronic drought at the time of our data collection. Since drought stress did not differ among tree locations, it is likely that other factors regulate M. tenebricosa within urban areas.

Habitats with greater plant structural complexity or diversity generally have more natural enemies or higher rates of parasitism than simple habitats (Andow, 1991; Langellotto and

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16 over M. tenebricosa we would have expected lower densities on landscape trees than forest trees. We did not assess generalist predatory arthropods which may also contribute to biological

control of scale insects. However, our findings corroborate those of Dale and Frank (2014b), who found that natural enemies do not regulate M. tenebricosa in urban landscapes where its fecundity and survival are also greater (Dale and Frank, 2014b, Dale and Frank, 2017). The results of our observational experiments infer temperature as the driver of M. tenebricosa density. However, there are other confounding factors that may exist between sites which we have accounted for in our manipulative experiment.

The results of our manipulative study which paired potted saplings with mature urban trees reinforces that temperature is the main factor that influences scale abundance by controlling for variation in soil moisture, compaction, and nutrition. After a single generation, M.

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17 Latitude, in addition to the urban heat island effect, affects the temperature of an urban area such that low latitude cities are warmer than higher latitude cities. Mean annual

temperatures for Raleigh and Newark-Philadelphia as measured from weather stations which are centrally located among study sites are 16.1 °C and 13.2 °C respectively. We found that M. tenebricosa density was greatest in Raleigh landscapes which are 2.9 °C warmer than Newark-Philadelphia. Thus, background temperature can alter arthropod abundance directly but relative differences in temperature change how arthropods are affected by warming. For example, at low latitudes urban warming may drastically increase or decrease insect abundance, but at high latitudes the effect of warming is largely positive for temperate arthropods (Youngsteadt et al., 2017). Such was the case for increased voltinism by many European butterfly species (Altermatt, 2010) and for range expansions by Thaumetopoea pityocampa (pine processionary moth)

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18 We and others (Dale and Frank, 2014a, Dale and Frank, 2017; Youngsteadt et al., 2014), have found extreme differences in M. tenebricosa abundance across only 1.3–2.0 °C urban temperature gradient. The eastern United States is predicted to warm by 2–3 °C in the next 50– 100 years (George et al., 2007) and the average annual temperature difference between Raleigh and Newark-Philadelphia is 2.9 °C. Given that we have isolated temperature as the main factor which predicts M. tenebricosa density we can conclude that Raleigh may be an indicator of future pest density in Newark-Philadelphia. Evidence for this comes from Just et al. (2018), who surveyed M. tenebricosa abundance in street trees across 10 degrees of latitude in southeastern North America and found a hump-shaped distribution with greatest abundances in mid-latitude cities. To the extent that the urban heat island effect is coupled with background climate and future warming, it is also possible that mid-latitudes will become too warm to support chronic infestations of M. tenebricosa and the range of the pest may shift altogether northward. Our study cities likely differed in ways other than background climate, such as total area, human population density, and overall urban intensity. However, southern and midlatitude cities which differ in these factors all show similar relationships between temperature and M. tenebricosa abundance (Just et al., 2018) thereby corroborating the role of temperature as the primary driver of M. tenebricosa density in the present study.

Conclusions

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19 trees in the United States have been valued at roughly $2.4 trillion (Nowak et al., 2002) and should be managed to sustain and maximize their benefits. Our work shows that urban forest fragments buffer trees from the urban heat island effect and concomitant stress and pest

infestations in a warm mid-latitude city. The same buffering should also enhance the ecosystem services provided by trees (Meineke et al., 2016) growing in forest fragments. Therefore, in addition to preserving forest fragments, municipalities may be able plant trees in clusters to reduce the temperature immediately around trees and strive to increase total canopy cover to shade impervious surfaces and reduce the urban heat island effect city-wide.

We anticipate that future climate warming will result in greater M. tenebricosa density in high latitude cities. However, if urban trees can be kept healthy, through altered planting

practices or by preserving forest fragments during urban development, they may contribute even more to the urban environment and human well-being. For example, greater tree density creates a cooling effect in urban environments (Ng et al., 2012), which as we have demonstrated, is

important for reducing urban tree pest density but also for energy savings (McPherson et al., 2005). Tree density is also correlated with increased public living preference, ties among

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20 and total land area required to reduce pest density and boost tree health would optimize

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21

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Figure 2: The effect of tree location on mean Melanaspis tenebricosa density. (a) In December 2016, planted landscape trees (n=17) had three orders of magnitude more M. tenebricosa than fragment edge (n=17) or fragment interior (n=17) trees in Raleigh, NC. (b) There was no

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Chapter 2: Pests reduce benefits of warming for northern trees

Abstract

Climate warming is predicted to have a positive effect on growth of many temperate tree species but can also benefit tree pests by increasing survival and fecundity. Little is known about how the additive or interactive effects of warming on trees and their pests may influence tree growth, and therefore, ecosystem services. I combine an observational field experiment with a factorial common garden experiment to disentangle the effects of latitudinal climate, local temperature, and climate warming on pest density and tree growth. First, I sampled Quercus phellos trees growing in cool urban forest fragments and nearby warm ornamental landscapes for Parthenolecanium quercifex in mid and high latitude cities within the range of Q. phellos. Then in the common garden I infested northern and southern trees with northern and southern pests to test the hypotheses that climate warming will increase the density of P. quercifex and growth of Q. phellos. I found that Q. phellos growing in urban ornamental landscapes had greater P. quercifex densities than those growing in urban forests in both high and mid-latitude cities, and, that trees in mid-latitude landscapes, the warmest I sampled, had the greatest density of all. The common garden experiment showed that P. quercifex of northern origin attained greater densities than P. quercifex of local origin when relocated to Q. phellos planted in a mid-latitude common garden. I also confirmed the hypothesis that Q. phellos of northern origin will grow more than trees of local origin. Lastly, P. quercifex of northern origin, when exposed to warming, had a negative effect on tree growth regardless of tree origin. My results show that climate warming will benefit tree growth and tree pests so that the positive effects of warming on P. quercifex are likely to dampen or counter any boost that warming may provide to Q. phellos growth.

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35

Introduction

Predicting how trees and their pests will be affected by climate warming is an important challenge of global change research. Warming can have positive (Gunderson, Norby &

Wullschleger 2000) or negative (Doughty & Goulden 2008) effects on tree growth depending on the magnitude of warming and the latitudinal climate to which the trees are adapted. Warming may increase the growth of many temperate and boreal trees due to longer growing seasons, less winter damage, and higher physiological function, such as photosynthesis, as trees approach their thermal optimum (Way & Oren 2010). However, warming can also negatively affect tree growth, particularly if trees are adapted to warm climates and close to their thermal maximum (Wertin, McGuire & Teskey 2011). Tree growth in the tropics is generally reduced by warming (Clark et al. 2003; Feeley et al. 2007; Clark, Clark & Oberbauer 2010) because tropical tree species have a narrow thermal tolerance for photosynthesis which, when exceeded, greatly reduces CO2

assimilation and growth. (Doughty & Goulden 2008; Way & Oren 2010). Even temperate trees can be negatively affected by warming due to factors such as functional group (Carter 1996), flexibility of thermal tolerance (D’Arrigo et al. 2004; Reich & Oleksyn 2008), and proximity to the southern edge of their geographic range (Wertin, McGuire & Teskey 2011). Thus, the range of many tree species are expected to shift poleward as low latitude parts of their range become uninhabitable (Iverson & Prasad 1998; McKenney et al. 2007; Prasad, Matthews & Peters 2008), or as they are outcompeted by warm-adapted tree species with faster growth rates (Schmidtling 1994; Way & Oren 2010).

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36 mountain pine beetles (Dendroctonus ponderosa) is expanding (Raffa, Powell & Townsend 2013) and they have higher winter survival (Creeden, Hicke & Buotte 2014), and increased voltinism (Mitton & Ferrenberg 2012) due to climate warming. Mountain pine beetles attack trees en masse to overcome the constitutive and inducible defenses of the tree (Boone et al. 2011) and climate change, particularly heat and drought, reduce defensive capacity of trees and thus, the number of beetles required to colonize and kill the tree (Raffa et al. 2008; Bentz et al. 2010; Raffa, Powell & Townsend 2013). Likewise, higher temperatures play a role in the northward range expansion of the hemlock woolly adelgid (Adelges tsugae) in North America (Dukes et al. 2009) and the pine processionary moth (Thaumetopoea pityocampa) in Europe (Battisti et al. 2005) along with many other pests (Pureswaran, Roques & Battisti 2018).

Warming benefits insects in the high latitude portions of their ranges through increased survival and fecundity (Deutsch et al. 2008). As herbivore ranges expand, they encounter trees that may be naive to their herbivory or under stress due to climate warming.

Trees and their pests have different life spans and migration potential (Lawton 1995; Bale & Hayward 2010). Arthropods have short generation times and, behavioral dispersal mechanisms, therefore greater potential for adaptation to warming or migration to colonize warmed locations, than trees which have long generation times and slow dispersal. Thus, trees adapted to northern climates could face the simultaneous challenges of warming and pests that benefit from

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37 on trees originating from different latitudes is to grow them in a common location (Matyas 1996). I took the common garden approach a step further by also infesting trees with pests from different latitudes. By doing so I disentangled the potentially different effects of temperature on pests and tree growth.

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38 quercifex, when warmed by the southern climate, attain higher densities than southern P.

quercifex in its native climate.

Methods

To determine how the location of a tree affects its temperature, and P. quercifex density, I selected 26 Q. phellos in Raleigh, North Carolina, USA growing in urban landscapes (n = 13), and forest fragments (n = 13). I recorded temperature of each tree at 4-hour intervals from May 26, 2016 to September 26, 2016 with Thermochron iButton data loggers DS1921G (Dallas Semiconductor, Dallas, TX). To avoid inflated temperature readings caused by exposure to direct sunlight, the data loggers were positioned in the lower canopy of study trees. I used the average of temperature readings across the 123 active days to obtain the mean temperature of each tree and analyzed with a t-test specifying average temperature as the dependent variable and tree location as the independent variable. I analyzed P. quercifex density by randomly pruning two 30 cm long twigs from opposite sides of each tree canopy between March 14-15. All live P. quercifex nymphs were counted on each twig and the sum was divided by 30 cm to obtain P.

quercifex density. I used the average of densities from the two twigs per tree for a measure of tree-level P. quercifex density. Between March 6-9, 2017 I sampled more Q. phellos from urban forest fragments (n=21) and urban landscapes (n=22) in Raleigh using the same methods as above. I also sampled Q. phellos in urban forest fragments and urban landscapes in Newark, DE, 502.9 km and 3.85 degrees latitude higher than Raleigh, between March 25-26, 2017.

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39 variable and tree location the predictor variable. I used Dunn all pairs posthoc significance tests to assess multiple comparisons between tree locations. These and all other analyses were conducted using JMP (‘JMP® Pro, Version 13.0.0. SAS Institute Inc., Cary, NC, 1987–2007’) statistical software.

I obtained the daily averages of 30-year climate data (1981-2010) from weather stations near the sources of all Q. phellos and P. quercifex as well as near the common garden itself from the National Oceanic and Atmospheric Administration’s Climate Data Online web portal

(https://www.ncdc.noaa.gov/cdo-web/). I used ANOVA to determine the difference in average annual temperature among the sources and the common garden. I specified the daily average temperature as the response variable and the source as the categorical predictor variable. I used Tukey’s HSD to test for pairwise differences in average temperature among the sites.

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40 On May 4, 2017, I collected gravid P. quercifex from four highly infested Q. phellos trees on the campus of North Carolina State University in Raleigh, NC to be used as the warm-adapted southern origin scales. On June 1, 2017 I collected cool-adapted northern origin scales from four highly infested Q. phellos at Glassgow Regional Park in Newark, DE. I infested the saplings with P. quercifex by fastening twigs with two gravid adults per 30 cm of height to the stems of the potted saplings using twist-ties. Different treatments were kept on separate tables in a greenhouse until P. quercifex nymphs had hatched and settled on the foliage. I counted the number of P. quercifex nymphs per leaf on 5 randomly selected leaves per tree and calculated the area of each leaf so that I could obtain the density of P. quercifex per tree. I measured sapling diameter 15 cm above the soil line and marked the location of the measurement with a permanent marker so that future measurements could be taken at the same point. In June 2017, I planted the saplings in a randomized grid pattern, spaced 2.1 meters apart, in the common garden. Trees were watered for 30 minutes every night using automatic sprinklers from late June to early October. P. quercifex density was calculated again, using the same methods outlined above, in July 2017, August 2017, June 2018, July 2018 and September 2018 spanning two generations. I calculated the density of adult P. quercifex by counting the number of gravid adults present in May 2018 and dividing it by the height of the tree. I remeasured the diameter of each tree at the end of the growing season in October 2018. I calculated the total diameter growth for each tree by subtracting the initial diameter from the October 2018 diameter.

To test the effects of warming on northern P. quercifex density I modeled P. quercifex nymph and gravid adult density (log(x+1)) using linear mixed effects models separately. I

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41 quercifex density (June 2017) as a covariate to account for potential differences in fecundity between southern and northern P quercifex. To determine how warming affected tree growth, I analyzed diameter growth (log(x+1)) using a mixed effects model. I specified Q. phellos origin, P. quercifex origin, their interaction, and the initial diameter of each tree at the time of planting as fixed effects and tree ID as a random effect. I included the initial diameter of the study trees as a covariate because trees with larger diameters are known to grow more in other systems (da Silva et al. 2002; McLaren et al. 2011). By relocating trees and pests from northern latitudes to a common garden at southern latitude I emulated the effects of climate warming on them. I then compared the density of pests and growth of trees which were naïve to the warm climate to trees and pests which were adapted to the common garden climate.

Results

Local and Latitudinal Effects of Temperature on P. quercifex:

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42 landscape trees (Z=-2.86, P=0.025). Like 2016, Raleigh forest fragments also had lower density of P. quercifex than Raleigh urban landscape trees (Z=-4.02, P<0.001). Newark forest fragments had lower P. quercifex densities than Raleigh landscape trees (Z=-5.72, P<0.001). There were no differences in P. quercifex density between Newark forest fragments and Raleigh forest

fragments (Z=-1.54, P=0.733) or Newark urban landscapes and Raleigh forest fragments (Z=1.25, P=0.999) (Figure 1).

The annual temperatures near the points of origin for northern and southern P. quercifex and Q. phellos differed (F4,1820=20.39, P<0.001) such that northern P. quercifex and Q. phellos were adapted to a climate that was on average 3.12 ºC (± 0.30 SEM) cooler than southern P. quercifex and Q. phellos (Figure 2). There was no difference in the average annual temperature for northern P. quercifex and Q. phellos. Nor was there a difference in annual temperature among the sources of southern P. quercifex, Q. phellos, and the common garden. But, since the average temperature at the northern latitudes was cooler than the southern latitudes it substantiates my use of a common garden to emulate climate warming on naïve trees and pests.

Parthenolecanium quercifex Density:

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43 quercifex (Figure 3) (Table 2). The effects of Q. phellos origin and the interaction between Q. phellos and P. quercifex origin were not significant.

Quercus phellos Growth:

The main effects of Q. phellos and P. quercifex origin each had a significant effect on diameter growth such that the northern trees grew more than southern trees and trees infested with northern scales grew less than those infested with southern scales. The main effect of initial diameter and the interaction between tree origin and scale origin were not significant (Figure 4) (Table 3).

Discussion

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44 latitudinal temperature. Therefore, a controlled experiment was necessary to strengthen my conclusion. I found that density of the northern origin P. quercifex was greater than the southern origin regardless of whether it was paired with a tree of northern or southern origin (Table 2, 3) when grown in the common garden. Arthropods from higher latitudes suffer greater winter mortality than their congeners from lower latitudes (McAvoy et al. 2017) and may compensate by having greater body size and fecundity (Blanckenhorn & Demont 2004). In fact, initial density, which I measured less than two weeks after egg hatch, influenced P. quercifex density, suggesting that northern P. quercifex were more fecund than southern. Furthermore, Meineke et al. (2013) found that warming of P. quercifex from a local cool source showed a general increase in abundance due only to differences in survival over the course of one growing season. My results corroborate broader theory that warming is likely to benefit insects in the northern part of their geographic range (Bale et al. 2002; Karban & Strauss 2004; Deutsch et al. 2008) due to enhanced survival and fecundity, and that warming specifically benefits P. quercifex (Meineke et al. 2013, 2016; Meineke & Frank 2018). Thereby, putting trees at risk as climate continues to warm.

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45 warm temperatures many more cells can be formed. In their study of eight deciduous tree species along an elevational gradient Lenz et al. (2014) found that basal area growth did not differ based on the length of the growing season except for trees growing near their range limit in warm years. The common garden was centrally located in the latitudinal range of Q. phellos and

northern origin trees were sourced from near the northern limit of Q. phellos range. The length of the growing season for northern trees in this study increased by 12 days (Diebel, Norda &

Kretchmer 2013) and the average temperature of the growing season increased by 2.9 ºC which falls within the range of warming predicted globally by 2100 (IPCC 2013). Therefore, I expect that the northern trees, which are biologically primed to take advantage of ephemeral warming, benefited compared to the climate-adapted southern trees especially given that soil nutrients and water availability were the same across all trees in the common garden.

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46 However, the trees in my study all received the same amount of water and northern P. quercifex density was greater regardless of tree origin. Which suggests that the effects of warming alone on Q. phellos of northern origin would not impose physiological changes in the trees that could have been detrimental to P. quercifex.

Parthenolecanium quercifex is a major pest of Quercus phellos in the southeastern United States (Frank 2019 in press) where Q. phellos is an important ornamental landscape tree. Global temperature is expected to continue increasing (IPCC 2013) and I have shown that as it does P. quercifex will become more problematic and therefore will require greater management

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48

References

Andrew, N.R., Hill, S.J., Binns, M., Bahar, M.H., Ridley, E. V., Jung, M.-P., Fyfe, C., Yates, M. & Khusro, M. (2013) Assessing insect responses to climate change: What are we testing for? Where should we be heading? PeerJ, 1, e11.

Bale, J.S. & Hayward, S.A.L. (2010) Insect overwintering in a changing climate. The Journal of experimental biology, 213, 980–94.

Bale, J.S., Masters, G.J., Hodkinson, I.D., Awmack, C., Bezemer, T.M., Brown, V.K.,

Butterfield, J., Buse, A., Coulson, J.C., Farrar, J., Good, J.E.G., Harrington, R., Hartley, S., Jones, T.H., Lindroth, R.L., Press, M.C., Symrnioudis, I., Watt, A.D. & Whittaker, J.B. (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biology, 8, 1–16.

Battisti, A., Stastny, M., Netherer, S., Robinet, C., Schopf, A., Roques, A. & Larsson, S. (2005) Expansion of the geographic range in the pine processionary moth caused by increased winter temperatures. Ecological Applications, 15, 2084–2096.

Bentz, B.J., Régnière, J., Fettig, C.J., Hansen, E.M., Hayes, J.L., Hicke, J.A., Kelsey, R.G., Negrón, J.F. & Seybold, S.J. (2010) Climate Change and Bark Beetles of the Western United States and Canada: Direct and Indirect Effects. BioScience, 60, 602–613. Blanckenhorn, W.U. & Demont, M. (2004) Bergmann and Converse Bergmann Latitudinal

Clines in Arthropods: Two Ends of a Continuum? Integrative and Comparative Biology, 44, 413–424.

Figure

Figure 1: The effects of tree location on canopy temperature and water potential are illustrated
Figure 2: The effect of tree location on mean Melanaspis tenebricosa density. (a) In December
Figure 3: Effect of tree position on parasitoid wasp abundance. The total number of parasitoid
Figure 4: Effect of tree position on Melanaspis tenebricosa density. Potted saplings that were
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References

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