University of Kentucky University of Kentucky
UKnowledge UKnowledge
Theses and Dissertations--Entomology Entomology
2017
A NON-NATIVE FOREST INVADER ALTERS FOREST STRUCTURE A NON-NATIVE FOREST INVADER ALTERS FOREST STRUCTURE
AND THE ASSOCIATED ARTHROPOD COMMUNITY AND THE ASSOCIATED ARTHROPOD COMMUNITY
Matthew B. Savage University of Kentucky, [email protected] Digital Object Identifier: https://doi.org/10.13023/ETD.2017.376
Right click to open a feedback form in a new tab to let us know how this document benefits you. Right click to open a feedback form in a new tab to let us know how this document benefits you.
Recommended Citation Recommended Citation Savage, Matthew B., "A NON-NATIVE FOREST INVADER ALTERS FOREST STRUCTURE AND THE ASSOCIATED ARTHROPOD COMMUNITY" (2017). Theses and Dissertations--Entomology. 41. https://uknowledge.uky.edu/entomology_etds/41
This Master's Thesis is brought to you for free and open access by the Entomology at UKnowledge. It has been accepted for inclusion in Theses and Dissertations--Entomology by an authorized administrator of UKnowledge. For more information, please contact [email protected].
brought to you by COREView metadata, citation and similar papers at core.ac.uk
provided by University of Kentucky
STUDENT AGREEMENT: STUDENT AGREEMENT:
I represent that my thesis or dissertation and abstract are my original work. Proper attribution
has been given to all outside sources. I understand that I am solely responsible for obtaining
any needed copyright permissions. I have obtained needed written permission statement(s)
from the owner(s) of each third-party copyrighted matter to be included in my work, allowing
electronic distribution (if such use is not permitted by the fair use doctrine) which will be
submitted to UKnowledge as Additional File.
I hereby grant to The University of Kentucky and its agents the irrevocable, non-exclusive, and
royalty-free license to archive and make accessible my work in whole or in part in all forms of
media, now or hereafter known. I agree that the document mentioned above may be made
available immediately for worldwide access unless an embargo applies.
I retain all other ownership rights to the copyright of my work. I also retain the right to use in
future works (such as articles or books) all or part of my work. I understand that I am free to
register the copyright to my work.
REVIEW, APPROVAL AND ACCEPTANCE REVIEW, APPROVAL AND ACCEPTANCE
The document mentioned above has been reviewed and accepted by the student’s advisor, on
behalf of the advisory committee, and by the Director of Graduate Studies (DGS), on behalf of
the program; we verify that this is the final, approved version of the student’s thesis including all
changes required by the advisory committee. The undersigned agree to abide by the statements
above.
Matthew B. Savage, Student
Dr. Lynne Rieske-Kinney, Major Professor
Dr. Charles Fox, Director of Graduate Studies
A NON-NATIVE FOREST INVADER ALTERS FOREST STRUCTURE AND THE ASSOCIATED ARTHROPOD COMMUNITY
THESIS
A thesis submitted in partial fulfillment of the requirements for the degree of Master of Science in the
College of Agriculture, Food and Environment at the University of Kentucky
By
Matthew B. Savage
Lexington, Kentucky
Director: Dr. Lynne Rieske-Kinney, Professor of Entomology
Lexington, Kentucky
2017
Copyright © Matthew B. Savage 2017
ABSTRACT OF THESIS
A NON-NATIVE FOREST INVADER ALTERS FOREST
STRUCTURE AND THE ASSOCIATED ARTHROPOD COMMUNITY The emerald ash borer (EAB, Agrilus planipennis Fairmaire) (Coleoptera:
Buprestidae) is a non-native wood boring beetle that is causing extensive ash (Fraxinus spp.) mortality in eastern North America, affecting both urban and wildland forests and drastically altering forest structure and composition. As EAB-induced ash mortality progresses, native arthropod associates of ash forests are impacted by the effects of rapid and broad scale tree mortality. These include loss of food source, increased canopy gap formation, alterations in litter inputs causing shifting temperature and moisture regimes on the forest floor, and significant accumulation of coarse woody debris.
I assessed the sub-canopy arthropod community in five forests, all in different stages of the invasion process, from introduction through impact. Additionally, I assessed the ground level arthropod community in a post EAB-invaded forest with 100% mature ash mortality. Arthropod communities were assessed at the ordinal level, and with a focus on coleopterans, they were further classified to families and trophic guilds to analyze abundance, richness, and diversity. Due to their overwhelming abundance, I identified scolytines collected in the post EAB-invaded forest to species to see if the EAB-invasion was part of a greater invasional meltdown. My results indicate that the EAB-invasion in North America is affecting the native coleopteran communities associated with these forests.
KEYWORDS: Agrilus planipennis, Fraxinus, invasive species, invasional meltdown, Scolytinae, trophic guild
Matthew B. Savage
July 12, 2017
A NON-NATIVE FOREST INVADER ALTERS FOREST
STRUCTURE AND THE ASSOCIATED ARTHROPOD COMMUNITY
By
Matthew B. Savage
Dr. Lynne Rieske-Kinney
Director of Thesis
Dr. Charles Fox
Director of Graduate Studies
July 12, 2017
Date
iii
ACKNOWLEDGEMENTS
This work has been possible thanks to the contributions of many individuals,
groups and institutions. I would first like to thank my advisor Dr. Lynne Rieske-Kinney
for believing in my potential and guiding me through my masters with her constant
support and advice. I would like to thank my past and current lab members, Abe Nielsen,
Ignazio Graziosi, Chris Strohm, Bill Davidson, Glenn Skiles, Sean Fenstemaker, and
Shouhui Sun for their friendship and all of their efforts in the lab and field. Thanks to our
undergraduate workers, Kyle Ritter, Jay Goldstein, Jeb Ayres, and Shane Stiles who
spent many long hours sorting through insect traps. Thanks to my research committee,
Dr. Mary Arthur and Dr. Lee Townsend, for their knowledgeable support to my research.
I would like to thank all of the landowners, Steve Martin, Lee Crawfort, Bonnie
Cecil, Taylorsville Lake State Park, Shelby County Parks and Recreation, and the
LFUCG staff at Raven Run Nature Sanctuary, for providing access to land for this
project. Thanks to Sarah Janse and Dr. Connie Wood for providing statistical support and
Dr. Eric Chapman for his expertise in beetle identification and his friendship. Funding
was provided by the USDA Forest Service Special Technology Development Program
and McIntire Stennis Funds from the Kentucky Agricultural Experiment Station.
Lastly, a special thanks to my parents, Kathy and Brian Savage, and Kelly
Jackson for their encouragement along the way.
iv
TABLE OF CONTENTS
ACKNOWLEDGEMENTS ............................................................................................... iii
TABLE OF CONTENTS ................................................................................................... iv
LIST OF TABLES ............................................................................................................ vii
LIST OF FIGURES ......................................................................................................... viii
CHAPTER 1: Introduction ................................................................................................. 1
CHAPTER 2: Coleopteran communities shift in response to emerald ash borer induced
ash decline in recently invaded forests ............................................................................... 5
Introduction ......................................................................................................... 5
Materials and Methods ........................................................................................ 6
Study Sites ...................................................................................................... 6
Forest Characteristics ...................................................................................... 7
Arthropod Monitoring ..................................................................................... 7
Analysis........................................................................................................... 8
Results and Discussion ....................................................................................... 9
Forest Characteristics ...................................................................................... 9
Arthropod Communities ............................................................................... 10
v
CHAPTER 3: Coarse woody debris accumulation associated with emerald ash borer-
induced ash mortality affects arthropod composition ....................................................... 20
Introduction ....................................................................................................... 20
Materials and Methods ...................................................................................... 22
Study Area .................................................................................................... 22
Coarse Woody Debris ................................................................................... 22
Arthropod Monitoring ................................................................................... 23
Analysis......................................................................................................... 24
Results ............................................................................................................... 26
Coarse Woody Debris ................................................................................... 26
Arthropod Monitoring ................................................................................... 26
Funnel traps ................................................................................................... 26
Pitfall traps .................................................................................................... 28
Pan traps ........................................................................................................ 29
Discussion ......................................................................................................... 30
APPENDICES .................................................................................................................. 45
APPENDIX A: Trophic guild designations ..................................................................... 46
vi
APPENDIX B: Temporal data by month.......................................................................... 48
APPENDIX C: CWD × Month treatment interactions ..................................................... 52
APPENDIX D: Scolytine abundance and origin .............................................................. 55
REFERENCES ................................................................................................................. 56
VITA ................................................................................................................................. 67
vii
LIST OF TABLES
Table 2.1, Forest characteristics and coleopteran abundance at five sites in north-central Kentucky used to evaluate changes in the colopteran community associated emerald ash borer-induced ash decline in 2014…14 Table 2.2, Relative abundance and richness of Coleopteran feeding guilds sampled from five sites affected by emerald ash borer ash decline……...15 Table 3.1, Effects of the presence of coarse woody debris and of season (Fdf/P) on coleopteran a) population parameters, b) feeding guild abundance, and c) family abundance sampled from funnel traps in EAB invaded forests of north-central Kentucky………………………………………..37 Table 3.2, Effects of the presence of coarse woody debris and of season (Fdf/P) on scolytinae species abundance (S.E.) sampled from funnel traps in EAB invaded forests of north-central Kentucky in 2015………………...39 Table 3.3, Effects of the presence of coarse woody debris and of season (Fdf/P) on coleopteran a) population parameters, b) feeding guild abundance, and c) family abundance sampled from pitfall traps in EAB invaded forests of north-central Kentucky………………………………………..41 Table 3.4, Effects of the presence of coarse woody debris and of season (Fdf/P) on coleopteran a) population parameters, b) feeding guild abundance, and c) family abundance sampled from pan traps in EAB invaded forests of north-central Kentucky………………………………………..43
viii
LIST OF FIGURES
Figure 2.1, Relative abundance of the ten numerically dominant coleopteran families found in forests under evaluation for emerald ash borer-induced ash mortality……………………………………………...16 Figure 2.2, Cumulative coleopteran family richness at five forested sites in north central Kentucky in 2014…………………………………………..17 Figure 2.3, Coleopteran feeding guild absolute abundance related to ash canopy decline (least to greatest) at five forested sites in north central Kentucky…………………………………………………………18 Figure 2.4, Correlation between Fraxinus canopy decline and absolute abundance of two coleopteran predators…………………………………19 Figure 3.1, Layout of plots, traps, and trap types used to evaluate the arthropod community associated with ash coarse woody debris in emerald ash borer-impacted forests……………………………………………….35 Figure 3.2, Volume (m3/0.1 ac.) of ash coarse woody debris in each decay class (mean (s.e.)) six years following invasion of emerald ash borer…..36
1
CHAPTER 1
Introduction
Non-native species’ invasions threaten forest ecosystem function (Ehrenfeld
2010) and native biodiversity (Wilcove et al. 1998, Byers et al. 2002), often with
widespread and devastating economic impacts (Pimentel et al. 2005, Aukema et al.
2011). Insect outbreaks can kill plants and alter the distribution of biomass over large
areas (Wilcove et al. 1998, MacLean 2002, Breshears et al. 2005, Kurz et al. 2008,
Brown et al. 2010), and also cause disturbance-induced changes in trophic interactions
(Schowalter 1985, Schowalter and Lowman 1999).
The emerald ash borer (Agrilus planipennis Fairmaire, EAB, Coleoptera:
Buprestidae) is a wood-boring beetle native to east Asia, which was first detected in
North America in 2002 near Detroit, MI (Haack et al. 2002). Larvae feed just below the
bark on the phloem of ash trees (Fraxinus spp.), forming serpentine galleries that destroy
vascular tissue and disrupt the translocation of water and nutrients to the canopy. This
ultimately girdles the tree, leading to rapid mortality (Cappaert et al. 2005, Flower et al.
2013). All North American Fraxinus, even healthy trees, are susceptible to EAB
(Cappaert et al. 2005), though blue ash, F. quadrangulata, demonstrates some putative
resistance (Tanis and McCullough 2012). Since its introduction, EAB has spread rapidly
through much of the eastern contiguous US and southeastern Canada (USDA APHIS
2017), and inflicted extensive ash mortality in affected regions. The EAB invasion in
North America is of unprecedented scope and magnitude (Herms and McCullough 2014),
and its effects are ultimately projected to be on a continental scale. The majority of EAB-
2
induced ash mortality (>85%) occurs within 3–5 years of an initial invasion (Poland and
McCullough 2006, Kashian and Witter 2011). However, following widespread
establishment residual populations may persist.
Ash trees are a consistent component of hardwood forests throughout the USA. In
addition to their economic value as a timber and landscape species, Fraxinus are
ecologically important as seed producers that provide valueable food resources for
wildlife (Kennedy 1990, Schlesinger 1990). Direct effects of the EAB invasion include
rapid ash mortality with subsequent alterations in ash-associated communities (Gandhi
and Herms 2010a). Specifically, ash tree mortality deprives many ash specialists of food
resources (Gandhi and Herms 2010b), though some species may thrive under the altered
conditions (Zhang and Liang 1995, Schowalter et al. 1999, Van Bael et al. 2004). The
indirect effects of rapid and broad scale tree mortality include increased canopy gap
formation, alterations in litter inputs causing shifting temperature and moisture regimes
on the forest floor, and significant accumulation of coarse woody debris (CWD) (Evans
2011, Perkins et al. 1987, Zhang and Liang 1995).
Increased coarse woody debris alters habitat heterogeneity, which can affect
arthropod communities through mechanisms such as increased exposure to predation and
parasitism (Shure and Wilson 1993, Van Bael et al. 2004). The increase in ash coarse
woody debris may have profound effects specifically on coleopteran community
associates, which are good indicators of disturbance (Schowalter and Ganio 2003) and
diversity (Hammond 1990), through altered habitats and resource distribution. These
habitat alterations could also facilitate invasions by other non–indigenous species,
creating an ‘invasional meltdown’ (sensu Simberloff and Holle 1999).
3
My research investigates the effects of EAB-induced ash mortality on arthropod
communities in invaded forests. I had two main objectives: (1) to evaluate arthropod
utilization of declining ash canopies during EAB invasions; (2) to evaluate arthropod
utilization of naturally occurring ash coarse woody debris post EAB invasion. I
completed my objectives through field experiments in six locations in east central
Kentucky over the course of two years.
In 2014, I monitored five locations in different stages of the invasion process from
introduction through impact. In chapter 2, I investigate the effects of EAB-induced ash
mortality on arthropod communities in invaded forests in different stages of the invasion
process. I predicted that EAB-induced ash mortality would lead to changes in forest
composition and structure resulting in shifts in arthropod communities. I compared the
arthropod activity across the five sites to determine any changes in arthropod
composition.
In 2015, I narrowed my focus to one county with three geographically distinct
study sites, where the EAB invasion had caused 100% ash mortality. In chapter 3, I
investigated arthropod utilization of naturally occurring ash coarse woody debris by
monitoring arthropods in plots with and without ash coarse woody debris. I predicted that
the influx of coarse woody debris due to EAB-induced ash mortality would create
additional habitat and resources resulting in changes in arthropod composition,
abundance, and richness.
Few studies have evaluated arthropod associates in EAB invaded forests, and a
clear understanding of the role of EAB induced ash mortality on forest arthropod
communities is lacking. By characterizing these effects on arthropod communities at
4
different stages of the EAB invasion, my research provides a greater understanding of the
impacts of the invasion and adds to the knowledge base surrounding arthropod
community structure following invasive species outbreaks. This is critical for conserving
native arthropod biodiversity following large-scale disturbance events.
5
CHAPTER 2
Coleopteran communities shift in response to emerald ash borer induced ash decline in
recently invaded forests
Introduction
Invasions by non-native invasive species pose significant threats to forest
ecosystem function (Ehrenfeld 2010) and native biodiversity (Wilcove et al. 1998, Byers
et al. 2002), and have widespread economic impacts (Pimentel et al. 2005, Aukema et al.
2011). Ash trees (Fraxinus spp.) are a consistent component of hardwood forests
throughout the United States (Kennedy 1990, Schlesinger 1990) whose prevalence and
persistence is threatened by the emerald ash borer (Agrilus planipennis Fairmaire, EAB,
Coleoptera: Buprestidae). This invasive wood-boring beetle is native to eastern Asia and
first detected in North America in 2002 near Detroit, MI (Haack et al. 2002). Since its
accidental introduction, EAB has rapidly spread through much of the eastern contiguous
United States and southeastern Canada (USDA APHIS 2016) inflicting extensive ash
mortality in affected regions. Larvae feed on phloem beneath the bark, forming
serpentine galleries and destroying the vascular tissue, disrupting translocation of water
and nutrients to the canopy, ultimately girdling the tree (Cappaert et al. 2005, Flower et
al. 2013). The majority of EAB-induced ash mortality (>85%) occurs within 3–5 years of
the initial invasion (Poland and McCullough 2006, Kashian and Witter 2011). All North
American Fraxinus species are susceptible to attack and EAB readily colonizes healthy
trees (Cappaert et al. 2005).
6
The direct effects of the EAB invasion include rapid ash mortality with
subsequent alterations in ash-associated communities (Gandhi and Herms 2010a). The
indirect effects of rapid and broad scale tree mortality include increased gap formation,
which alters light penetration to the forest floor, accumulation of coarse woody debris,
and qualitative and quantitative alterations in litter inputs causing shifting temperature
and moisture regimes on the forest floor (Perkins et al. 1987, Zhang and Liang 1995).
Such changes after EAB-induced ash mortality may affect native coleopteran community
associates of these invaded forests. My goal is to document how these native coleopteran
communities shifted in response to EAB-induced ash mortality in recently invaded areas
of the east central United States. Specifically I evaluated the extent to which coleopteran
trophic guild abundance and richness were affected by widespread EAB-induced ash
mortality.
Materials and Methods
Study Sites
Five forested study sites were established in north-central Kentucky along the
forefront of the expanding EAB infestation (Davidson and Rieske 2015), in Anderson,
Fayette, Henry, Shelby, and Spencer counties. Ash are historically a significant
component of the western mesophytic forests of the region (Wharton and Barbour 1973),
which thrive on the moist and fertile soils that predominate in this area (Campbell 1989).
At the onset of the study EAB was present at the Anderson, Henry, and Shelby sites
where ash decline was evident. EAB was first detected at Fayette and Spencer sites in
2014, but there were little to no signs of EAB-induced stress (Davidson and Rieske
2015). My sites were chosen to represent the full spectrum of ash decline associated with
7
the EAB invasion, including pre-invasion (Fayette, Spencer), peak invasion (Shelby), and
post-invasion (Henry, Anderson) forests.
Forest Characteristics
Forest vegetation was characterized at each site to determine pre-invasion
conditions and annually thereafter. For vegetation censusing, nine circular whole plots
(0.04 ha) were utilized to assess overstory and midstory vegetation (all trees ≥ 12.7 cm
diameter at 137 cm high; DBH), 0.004-ha subplots were used to assess saplings and
shrubs (< 12.7 cm DBH, > 137 cm high), and 0.0004-ha microplots were used to assess
seedlings and shrubs (< 137 cm height). One subplot and one microplot were positioned
at the whole plot center and in each cardinal direction, 7.7 m from the whole plot center.
Thus, a surveyed plot contained one 0.04-ha whole plot, five 0.004-ha subplots, and five
0.0004-ha microplots (Coleman et al. 2008). Measurements of vegetation and plot data
followed the Common Stand Exam protocol of the USDA Forest Service’s Natural
Resource Information System: Field Sampled Vegetation Module (USDA Forest Service
2009) and included tree height and DBH. Canopy dieback was visually assessed by a
single observer and each ash tree assigned a crown dieback rating from 0% (healthy) to
100% (dead).
Arthropod Monitoring
Native coleopteran communities in the sub-canopy strata were monitored using
12-unit Lindgren multi-funnel traps (one per plot, N=45) from 20 May to 12 September
2014. Traps were suspended over an ash branch (~4 m) and fitted with two 50 ml vials of
70% ethanol, a commonly used lure for xylophagous insects (Montgomery and Wargo
1983, Lindelöw et al. 1992, Bouget et al. 2009), hung from the funnel edge, and with a
8
dichlorvos strip (2 × 5 cm2) (AMVAC Chemical Corp., Los Angeles, CA) placed in each
trap bottom. Traps were monitored every 7-14 d; contents were rinsed and stored in 70%
EtOH in resealable plastic bags, and the lures replenished. In the laboratory samples were
sorted to order (Triplehorn and Johnson 2005); Coleoptera were further sorted and
identified to family using available keys (Triplehorn and Johnson 2005, Marshall 2006,
Evans 2014, BugGuide 2015), counted, and assigned to trophic guilds based on larval
feeding habits, including fungivore, predator, herbivore, xylophage, saprophage, or
parasitoid, (Hammond 1990). Ordinally the Coleoptera are trophically diverse, but more
or less trophically uniform within families (Hammond 1990, Hammond 1992), which
allows classifying families into feeding guilds that exploit resources in a similar manner
(Root 1967). In my study the carrion feeders, including some Silphidae, Staphylinidae,
Histeridae, Nitidulidae, and Lieodidae, were responding to the decaying trap contents
rather than the ethanol lure, which resulted in excessive fluctuations in abundance, and so
were excluded from my analyses.
Analysis
Ash decline, characterized by 2014 canopy dieback (Table 2.1), was compared
across all sites using a one-way analysis of variance (ANOVA), with post hoc analysis
performed using Tukey’s Honest Significant Difference (HSD) (Davidson and Rieske
2015). Ash canopy dieback ranging from low (Fayette) to high (Henry) was then used to
assess the influence of ash decline on coleopteran abundance and richness. Coleopteran
abundance measured with funnel traps (recorded as total Coleoptera trapped) was
calculated and richness (recorded as total number of coleopteran families trapped) was
derived by site. Evenness and diversity indices were not derived due to data gaps. Data
9
were tested for normality (PROC UNIVARIATE) and transformed when necessary.
Significance was determined at α = 0.05 unless stated otherwise. All analyses were
performed using SAS v9.3 (SAS Institute 2011).
Overall coleopteran abundance and cumulative richness by site were analyzed
using a repeated measures mixed linear model (PROC MIXED), with sample interval as
the repeated measure and individual plots (traps) as subjects. The difference of least
squares (Least Squares Means) was used to separate means for these population
parameters. Coleopteran feeding guild abundance and richness summed over the 16 week
sampling period were analyzed using a generalized linear mixed model (PROC GLM) to
compare guild × site interactions. Feeding guild abundance was transformed using a
square root transformation for total counts and arcsin transformation for percent
abundance. Feeding guild abundance (absolute and percent) was compared across all sites
where the difference of least squares was used to separate means and post-hoc analysis
was performed using pairwise T-Comparison if differences arose. Correlations between
the predator guild and ash canopy decline were analyzed (PROC CORR).
Results and Discussion
Forest Characteristics
Across my study sites ash relative stem density ranged from 12-26% for stems
>2.5 cm diameter, and ash mortality ranged from 0-50%. Ash canopy dieback differed
significantly across sites, and ranged from a low of ~7% at the most recently invaded site
to a high of 74% at the most degraded site (Table 2.1). Site level ash mortality and
canopy dieback were highly correlated with EAB abundance (Davidson and Rieske
2015).
10
Arthropod Communities
Funnel traps yielded 16,455 arthropods, including 11,786 coleopterans (>71%)
representing 57 families, excluding carrion feeders (Appendix 1). Elateridae was the most
abundant family (Fig. 2.1), with 16% of the total, followed by the Curculionidae and
Staphylinidae (13 and 12%, respectively); these three families comprised nearly 41% of
the coleopterans captured. The next most abundant families were the Ptilodactylidae
(9%), the Latridiidae (9%), and the Histeridae (8%); collectively they comprised almost
27% of the total coleopterans.
Coleopteran abundance (Table 2.1), but not cumulative family richness (Fig. 2.2)
differed among study sites; both tended to be lowest in pre- (Fayette) and post-invasion
(Henry) sites, and greatest at the site typifying peak invasion (Shelby). The increase in
abundance and cumulative richness of coleopteran associates at the site representing the
peak of the EAB invasion may be attributable to increases in habitat availability due to
newly forming snags and coarse woody debris and to volatiles released from dying trees
(Kimmerer and Kozlowski 1982, Montgomery and Wargo 1983, Harmon et al. 1986).
Coleopteran abundance was greatest among herbivores (4,207 individuals, 36%)
(Table 2.2), comprised primarily of the Elateridae, which feed on flowers, nectar, pollen,
and rotting fruit (Evans 2014). However, in spite of their abundance herbivores
comprised only 14% of the total with respect to family richness (8 families). In contrast,
coleopteran fungivore richness was highest at 40% (23 families), in spite of the fact that
abundance was relatively low (2,082 individuals, 17%) (Table 2.2). Fungivores are
dominated by the Latridiidae (Fig. 2.1), which typically feed on the reproductive
structures of fungi and are commonly found in plant debris (Evans 2014). Predators
11
comprised 26% of the total (3,050 individuals) and 19% of the coleopteran family
richness (11 families) (Table 2.2). Predators consisted primarily of the Staphylinidae
(Fig. 2.1), which are generalist predators, and the Histeridae, which has one subfamily
associated with bark beetle (Curculionidae) galleries, and another subfamily that feeds
principally on fly and beetle larvae associated with dung. Saprophages and xylophages
made up ~10% of the abundance, and similarly 10 and 12% of coleopteran family
richness, and consisted primarily of Ptilodactylidae and Scolytines (Fig. 2.1; Table 2.2).
Trophic guild abundance across sites varied (χ2 = 1,045.6; df = 20; P < 0.0001),
corresponding to levels of EAB-induced ash decline. Herbivore and saprophage
abundance was greatest at Shelby (Figs. 2.3a and 2.3b), which among the five sites
represents peak EAB invasion. Fungivore abundance (Fig. 2.3c) was positively
associated with ash decline and was greatest at Shelby, Anderson, and Henry, where the
EAB invasion is more advanced, and lowest at Fayette and Spencer, which were in the
very early stages of the invasion at the time of sampling. Xylophages were most abundant
at Spencer (Fig. 2.3d), again representing relatively early stages of EAB invasion.
Predator abundance (Fig. 2.3e) was lowest at Fayette and Henry, representing both pre-
and post-EAB invasion and highest at the sites where the invasion is nearer its peak.
Among the predators, Trogossitidae and Cleridae abundance (7 and 5% of total
predator abundance, respectively) were positively correlated with ash decline (α < 0.1)
(Fig. 2.4). Trogossitids consisted of 228 individuals of primarily Tenebroides sp.; these
are bark-gnawing beetles found beneath the bark of dead trees and are associated with
wood-boring beetles (Evans 2014). Clerids (144 individuals) consisted primarily of
Enoclerus sp.; these checkered beetles are associated with dead wood, and often found
12
predating larval Curculionidae, Cerambycidae, and Buprestidae (Evans 2014).
Interestingly, the parastic Passandridae, comprised entirely of Catogenus rufus
(Fabricius), were consistently present in low numbers, regardless of ash decline
(Appendix 1). Catogenus rufus (Fabricius) has been reported in association with EAB-
invaded forests and has been found as both larvae and adults in EAB galleries from dead
ash on these sites (Davidson and Rieske 2015); it was present in low numbers across sites
(Fig. 2.3f) and appeared unaffected by the stage of the EAB invasion or by the
corresponding decline in ash canopies. Its presence at all sites in similar abundance
suggests that it is capable of utilizing a variety of wood-boring hosts and is not
demonstrating a numerical response to the EAB invasion in these forests, although it may
be utilizing EAB as a prey resource. Tenebroides, Enoclerus and Catogenus have been
documented in association with EAB larvae and pupae near the epicenter of the EAB
invasion in North America (Bauer et al. 2004), suggesting that they may be playing a role
in population dynamics of this aggressive invader. Collectively, these data suggest that
native predators and parasites are being recruited to invading emerald ash borer
populations, and that these native natural enemies may be a viable component of post-
invasion EAB population dynamics in North American forests.
The reverberating effects of the emerald ash borer invasion in North America will
undoubtedly include effects on native arthropod associates. Changes in forest structure
and composition, alterations in light penetration to the forest floor, and inputs of coarse
woody debris create and eliminate habitats and affect resource availability. Ash-
dominated forests are predicted to have a loss of overall arthropod richness, are facing
cascading ecological impacts, and altered ecosystem processes (Gandhi and Herms
13
2010b). Of the 282 native arthropods associated with ash, 43 are monophagous; nine of
these monophages are coleopterans (Gandhi and Herms 2010b). These ash specialists will
undoubtedly be negatively affected and may experience localized extirpation.
The emerald ash borer devastates unprotected ash. Following depletion of the ash
resources, EAB populations sharply decline (Herms and McCullough 2014), greatly
reducing the pest pressure on regenerating seedlings and saplings. The decline in pest
pressure increases the chance of continued survival of young ash in North American
forests (Duan et al. 2015), providing essential resources for ash specialists. Ash forests
are changing, and a deeper understanding of how arthropod communities and trophic
guilds are responding will contribute to more proficient monitoring and protection.
Table 2.2. Forest characteristics and coleopteran abundance at five sites in north-central Kentucky used to evaluate changes in the
colopteran community associated emerald ash borer-induced ash decline in 2014.
Fraxinus spp.
Site
No. stems
(all spp.)
No. stems
%
% mortality
Canopy dieback
mean % (SE)
Coleoptera
abundance1
Henry 466 79 18.5
50.5 73.9 (4.6)a 1.30 (0.07)b
Anderson 402 53 18.8 18.9 56.9 (1.9)b 1.53 (0.07)ab
Shelby 385 121 26.0 7.4 27.4 (3.9)c 1.64 (0.06)a
Spencer 290 59 12.0 1.7 16.2 (2.8)cd 1.49 (0.11)ab
Fayette 267 42 13.1 0.0 7.4 (3.0)d 1.27 (0.08)b
F3, 350 58.6; P<0.001 F4, 527 2.1; P<0.02
1LS-means + se number of individuals per day captured in ethanol-baited funnel traps. Means separation on square root + 0.05
transformed data.
14
15
Table 2.2. Relative abundance and richness of Coleopteran feeding guilds sampled from
five sites affected by emerald ash borer ash decline.
Coleopteran family-level
Trophic guild Abundance (%) Richness (%)
Herbivore 36 14
Fungivore 17 40
Predator 26 19
Xylophage 10 12
Saprophage 10 10
Parasite <1 5
Unidentified <1 ---
Total 100 100
16
Figure 2.1. Relative abundance of the ten numerically dominant coleopteran families
found in forests under evaluation for emerald ash borer-induced ash mortality.
02468
101214161820
Col
eopt
eran
Fam
ily A
bund
ance
(%)
17
Figure 2.2. Cumulative coleopteran family richness at five forested sites in north central
Kentucky in 2014.
25
30
35
40
45
50
1 3 5 7 9 11 13 15
Cum
ulat
ive
Fam
ily R
ichn
ess
Weeks
FayetteSpencerShelbyAndersonHenry
May June July Aug. Sept. Oct.
18
Figure 2.3. Coleopteran feeding guild absolute abundance related to ash canopy decline
(least to greatest) at five forested sites in north central Kentucky, including a) herbivores,
b) saprophages, c) fungivores, d) xylophages, e) predators, and f) parasitoids. Means
followed by same letter do not differ (α=0.05).
19
Figure 2.4. Correlation between Fraxinus canopy decline and absolute abundance of two
coleopteran predators, including the Trogossitidae (Trogossitid abundance = 0.47 × (%
canopy decline) + 28.7, R2 = 0.84, P = 0.07) and the Cleridae (Clerid abundance = 0.45 ×
(% canopy decline) + 12.5, R2 = 0.86, P = 0.06).
0
10
20
30
40
50
60
70
80
0 10 20 30 40 50 60 70 80
Cole
opte
ran
Abso
lute
Abu
ndan
ce
Mean % Ash Canopy Decline
Trogossitidae AbundanceCleridae Abundance
20
CHAPTER 3
Coarse woody debris accumulation associated with emerald ash borer-induced ash
mortality affects arthropod composition
Introduction
Natural disturbances, including insect outbreaks, can extensively alter habitat
conditions and resource distribution across landscapes (White and Pickett 1985, Walker
1999, Schowalter 2012). Insect outbreaks can kill plants and alter the distribution of
biomass over large areas (Wilcove et al. 1998, MacLean 2002, Breshears et al. 2005,
Kurz et al. 2008, Brown et al. 2010), and also cause disturbance-induced changes in
trophic interactions (Schowalter 1985, Schowalter and Lowman 1999). In both cases,
non-native insect outbreaks pose significant threats to forest composition and structure,
forest ecosystem function (Ehrenfeld 2010) and native biodiversity (Wilcove et al. 1998,
Byers et al. 2002), and have widespread economic impacts (Pimentel et al. 2005, Aukema
et al. 2011). Each disturbance event is characterized by a combination of type,
magnitude, frequency, and extent that determines its effect on various organisms (White
and Pickett 1985, Walker 1999). Of particular concern in the USA are disturbance events
caused by invasion by the non-native emerald ash borer (Agrilus planipennis Fairmaire,
EAB, Coleoptera: Buprestidae).
Emerald ash borer is a wood-boring beetle native to east Asia and first detected in
North America in 2002 near Detroit, MI (Haack et al. 2002). Larvae feed on phloem of
ash trees (Fraxinus spp.), forming serpentine galleries which destroy the vascular tissue,
disrupting translocation of water and nutrients to the canopy, and ultimately girdling the
21
tree (Cappaert et al. 2005, Flower et al. 2013). Since its introduction EAB has spread
rapidly through much of the eastern contiguous US and southeastern Canada (USDA
APHIS 2016) inflicting extensive ash mortality in affected regions. Ash are a consistent
component of hardwood forests throughout the USA (Kennedy 1990, Schlesinger 1990),
and North American Fraxinus, even healthy trees, are susceptible to EAB (Cappaert et al.
2005). The EAB invasion in North America is of unprecedented scope and magnitude
(Herms and McCullough 2014), and its effects are projected to be on a continental scale.
The majority of EAB-induced ash mortality (>85%) occurs within 3–5 years of the initial
invasion (Poland and McCullough 2006, Kashian and Witter 2011). However, following
widespread establishment residual populations persist.
EAB-induced ash mortality affects insect communities both directly and
indirectly. Direct effects include rapid ash mortality which deprives many ash specialists
of food resources (Gandhi and Herms 2010b), though some species may thrive under the
altered conditions (Zhang and Liang 1995, Schowalter et al. 1999, Van Bael et al. 2004).
Indirect effects include increased gap formation which alters light penetration to the
forest floor, qualitative and quantitative alterations in litter inputs causing shifting
temperature and moisture regimes (Perkins et al. 1987, Zhang and Liang 1995), and
accumulations of coarse woody debris (CWD). The influx of ash coarse woody debris
following EAB invasions is significant (Evans 2011), affecting habitat heterogeneity of
the forest floor and thus resource availability and exposure to predation and parasitism
(Shure and Wilson 1993, Van Bael et al. 2004). The increase in ash coarse woody debris
may have profound effects on coleopteran community associates, which are good
indicators of disturbance (Schowalter and Ganio 2003) and diversity (Hammond 1990),
22
through altered habitats and resource distribution. These habitat alterations from the EAB
invasion could facilitate invasion by other non–indigenous species, creating an
‘invasional meltdown’ (sensu Simberloff and Holle 1999), whereby non-indigenous
species facilitate one another’s invasion success through increased likelihood of survival,
ecological impact, and magnitude of impact (Simberloff and Holle 1999). My goal was to
evaluate how this localized influx of ash coarse woody debris affects native coleopteran
communities in post EAB-invaded forests of the east central United States, and to
document evidence suggesting the occurrence of an EAB-induced invasional meltdown.
Materials and Methods
Study Area
My study area was a 13.8 ha forested tract in western Franklin County, KY,
which had been invaded by EAB since 2009. Historically ash were a significant
component of the western mesophytic forests of the region (Wharton and Barbour 1973),
which thrive on the moist and fertile soils that predominate in this area (Campbell 1989).
Initially ash comprised ~10 percent of the woody plant composition at the site, but at the
onset of my study in fall 2014 ash mortality was approaching 100% (Levin-Nielsen and
Rieske 2014). This EAB-induced ash mortality resulted in large accumulations of
naturally occurring coarse woody debris, woody material >2.5 cm in diameter, of varying
age, size, and state of decomposition.
Coarse Woody Debris
In October 2015 three discrete areas were designated containing six 0.04 ha whole
plots; three were designated as ash CWD present (CWD+), and three were designated as
ash CWD absent (CWD–). Within the CWD– plots, all ash CWD was carefully removed
23
and placed well outside the 0.04 ha plot boundary. Within the CWD+ plots the ash CWD
was carefully condensed into a central subplot and placed so as to maximize contact with
the ground. The length and diameter at both ends of all ash >2.5 cm diameter were
measured and assigned to a decay class (Vanderwel et al. 2006), which included (1) wood
hard, bark intact; (2) wood hard, bark beginning to slough; (3) wood softening, usually no
bark remaining; (4) wood substantially decayed, pieces sloughing off, inner heart wood
still intact; and (5) wood thoroughly decayed, texture powdery and resembles soil. To
calculate the amount of ash CWD present I recorded both small and large end diameter of
each piece to obtain an average diameter, then used the formula for a cylinder 𝑉𝑉 = 𝜋𝜋𝑟𝑟2ℎ
summed over all ash present to produce an ash CWD volume estimate, which is
expressed as m3 per plot. Ash CWD volume was also calculated for each decay class
(Fig. 3.2).
Arthropod Monitoring
To monitor associated EAB activity, green 12-unit multifunnel traps (N = 9)
affixed with manuka oil and leaf alcohol lures (Synergy, Brunbay, BC) were deployed
adjacent to study plots. Arthropod communities associated with the coarse woody debris
treatments were monitored from 21 March to 28 August 2014 using one 8-funnel trap (n
= 18) and two pairs of pitfall and pan traps (n = 36), spaced ~1 m apart equilaterally (Fig.
3.1). Funnel traps were mounted at a height of 1 m, and fitted with two 50 ml vials of
70% ethanol, a commonly used lure for xylophagous insects (Montgomery and Wargo
1983, Lindelöw et al. 1992, Zhang and Liang 1995, Bouget et al. 2009), hung from the
funnel edge, and with a dichlorvos strip (2 × 5 cm2) (AMVAC Chemical Corp., Los
Angeles, CA) placed in each trap cup. To sample surface and ground-dwelling
24
arthropods, pitfall traps were used consisting of two nested 473 ml plastic cups placed
into a hole flush with the soil surface and filled with ~100 ml of 1:1 70% ethanol:
ethylene glycol. A rain guard consisting of a clear 26 cm plastic plate was suspended ~3
cm above the trap using wire. To sample aerial arthropods and focusing on the
hymenoptera, pan traps were used consisting of two nested yellow 355 ml plastic bowls
(16 cm × 4 cm, Festive Occasion, East Providence, RI) with the internal bowl secured to
the outer bowl using binder clips and filled with ~75 ml soapy water. Traps were
mounted on 5 cm × 5 cm × 1 m wooden posts. Each trap type was deployed for 72 h
every 7 d. Following each deployment, contents were removed and strained through
paper filters (Rockline Industries, Sheboygan, WI), placed in sealable plastic bags with
70% ethanol, and stored at 4 °C until processing. In the laboratory arthropods were sorted
to order (Triplehorn and Johnson 2005) and counted. Coleopterans were further identified
to family (Marshall 2006, Evans 2014, BugGuide 2016). Coleopteran families are
relatively uniform trophically (Hammond 1990, Hammond 1992), which allows
classifying families into feeding guilds based on larval feeding behavior (Root 1967);
therefore I further assigned coleopteran families to trophic guilds based on larval feeding
habits, including fungivore, predator, herbivore, xylophage (including here xylomyceto-,
cambio-, and phloephagous members), saprophage, or parasitoid (Hammond 1990).
Scolytinae (Curculionidae) were further identified to species (Baker et al. 2009, Mercado
2010) and evaluated with respect to native vs non-native origin.
Analysis
The volume of CWD was compared across all decay classes in each plot using a
one-way analysis of variance (ANOVA), with a post hoc analysis using Tukey’s Honest
25
Significant Difference (HSD). For each monitoring approach, coleopteran abundance,
richness, diversity, and evenness were evaluated based on the presence of CWD.
Arthropod abundance measured with each trap type focused on coleopterans and was
analyzed by family and feeding guilds. Coleopteran diversity and richness were derived
for each sample approach (funnel, pitfall, and pan) within each plot. Richness is the total
number of taxa within a sample. Simpson’s diversity index utilizes the relative abundance
of each taxon and the total insect abundance within a sample (Magurran 2013), and is
calculated using 𝐷𝐷 = Σ𝑝𝑝𝑖𝑖2 𝑜𝑜𝑟𝑟 Σ 𝑛𝑛𝑖𝑖(𝑛𝑛𝑖𝑖−1)𝑁𝑁(𝑁𝑁−1)
. Shannon’s index, which utilizes both richness and
relative abundance and better represents my data consisting of many unique families with
low abundance, was also calculated using 𝐻𝐻′ = −Σ[(𝑝𝑝𝑖𝑖) ∗ 𝑙𝑙𝑙𝑙(𝑝𝑝𝑖𝑖)]. Evenness was
calculated using 𝐸𝐸 = 𝐻𝐻𝐻𝐻𝑚𝑚𝑚𝑚𝑚𝑚
𝑤𝑤ℎ𝑒𝑒𝑟𝑟𝑒𝑒 𝐻𝐻𝑚𝑚𝑚𝑚𝑚𝑚 = ln (𝑁𝑁) (Magurran 2013). Data over the 20-
week sampling period were grouped into five 4-week intervals (April, May, June, July,
and August) and summed. Data were tested for assumptions of normality (PROC
UNIVARIATE); abundance values were transformed using a square root transformation
to help reduce right skewness and because of many low and zero values. Significance
was determined at α = 0.05 unless stated otherwise. Arthropod abundance, richness,
Simpson’s and Shannon’s diversity indices, and Shannon’s evenness were analyzed using
a mixed linear model (PROC MIXED) to compare differences based on the presence or
absence of CWD and differences in time intervals (months) among coleopteran
population parameters, guilds, families, and scolytinae species (funnel traps only).
Sorenson’s index of similarity was computed to compare coleopteran family level
similarities between CWD+ and CWD–. All analyses were performed using SAS v9.3
(SAS Institute 2011).
26
Results
Coarse Woody Debris
The volume of ash coarse woody debris in the CWD+ plots averaged 0.7 m3,
whereas the volume in CWD– plots was 0. In CWD+ plots there were significant
differences in relative volume among decay classes (Fig. 3.2), with 89% (~0.62 m3) in
decay classes 1 and 2, and none present in decay class 5.
Arthropod Monitoring
All monitoring approaches collectively yielded 61,299 arthropods. Funnel traps
yielded 26,982 arthropods, including 24,107 coleopterans (89%) representing 54 families.
Pitfall traps yielded 16,878 arthropods, including 2,552 Coleoptera (15%) representing 30
families. Pan traps yielded 17,439 arthropods, including 2,864 Coleoptera (16%)
representing 46 families.
Funnel traps
In funnel traps there were no significant differences in overall coleopteran
abundance or evenness. However, coleopteran abundance was numerically greater in
association with ash CWD (11,560 in CWD+ vs. 8,663 in CWD–). Coleopteran family
richness and diversity (Shannon’s and Simpson’s) were significantly greater in the
presence of ash CWD (Table 3.1a). Similarly, there were significant temporal differences
in coleopteran population parameters, with a significant CWD × month interaction for
Simpson’s diversity index. Abundance was greatest in April and was driven by the sheer
number of xylophages (Appendix B.1(a)), which might also play a role in reducing
coleopteran evenness in April. Coleopteran family richness was greatest in June, and was
also significantly greater in the CWD+ treatment in June (p<0.01). Shannon’s diversity
27
was greatest in June and July, and Simpson’s diversity was greatest in May, June, and
July, and was significantly greater in the CWD+ treatment in August (p<0.01).
(Appendix C.1(a)).
There were significant differences in abundance between CWD treatments for
fungivores, herbivores, and saprophages captured in funnel traps; all three were
significantly more abundant in the presence of ash CWD, and the remaining feeding
guilds did not differ (Table 3.1b). Seasonal differences were evident for each guild (Table
3.1b). Fungivores were most abundant in April (Appendix B.1(b)). Herbivores were most
abundant in June and July, and saprophages in June. Saprophage abundance was also
significantly greater in association with ash CWD in June (p<0.01) (Appendix C.1(b))
Predator abundance followed a trend (p=0.07) of being greater in early spring and lower
at the end of the summer. Xylophages, consisting mainly of xylomycetophagous
scolytines, were significantly more abundant in April, with ~18,000 captured (Appendix
B.1(b)). Only seven parasitoids, represented by Catogenus rufus in the family
Passandridae, were captured in June and only in the funnel traps.
Of the 54 coleopteran families captured in funnel traps, 11 were significantly
more abundant in association with ash CWD and one was more abundant where ash
CWD was absent (Table 3.1c). Coleopteran abundance differed by month for most taxa
(Appendix B.1(c)), but only four taxa (Eucnemidae, Monotomidae, Ptilodactylidae, and
Silphidae) exhibited CWD × month interactions (Appendix C.1(c)). Sorenson’s index of
similarity of coleopteran families between CWD treatments equaled 0.90. The differences
among the coleopteran community in the CWD treatments included four unique families
in the CWD+ treatment, three of which were fungivores (Eucinetidae, Sphindidae, and
28
Throscidae) which feed on slime molds and basidiomycetes. There were six unique
families found in the absence of ash CWD; none were fungivores.
Of the 13 scolytinae species captured in funnel traps, none were significantly
different between CWD treatments (Table 3.2). This is likely because Scolytinae are
highly mobile; standing dead ash was scattered across the landscape and scolytines travel
large distances after emergence from infested trees. Scolytinae abundance differed by
month for most taxa (Table 3.2). Five taxa (Xyleborinus saxeseni, Ambrosiodmus
tachygraphus, Euwallacea validus, Monarthrum fasciatum, Xyleborus pelliculosus) were
significantly more abundant in April, and three taxa (Xyleborus ferrugineus, Xylosandrus
crassiuculus, Anisandrus sayi) were significantly more abundant in June (Appendix B.4).
Pitfall traps
Surprisingly, and in contrast to the funnel traps, Coleoptera activity density
measured by abundance in pitfall traps was significantly lower in association with ash
CWD (1,153 in CWD+ vs. 1,399 in CWD–), but there were no other differences in
population parameters between CWD treatments (Tables 3.4a). There were significant
temporal differences in coleopteran population parameters for all parameters, but there
were no significant CWD × month interactions. All population parameters were greatest
in June (Appendix B.2(a)).
Fungivore abundance in pitfall traps was significantly and unexpectedly lower in
association with ash CWD, and the remaining feeding guilds did not differ (Table 3.3b).
Seasonal differences were evident for each feeding guild. Fungivore abundance was
driven by the Nitidulidae, which were more abundant in the summer months.
29
Saphrophages were more abundant in June, predators in May and June, and xylophages
in April (Appendix B.2(b)).
Of the 30 coleopteran families captured in pitfall traps, Carabidae,
Chrysomelidae, and Nitidulidae were significantly more abundant where ash CWD was
absent. There was a weakly significant effect of CWD on Cryptophagidae and Elateridae;
these were more abundant in association with ash CWD present. (Table 3.3c).
Coleopteran abundance differed by month for most taxa and no taxa exhibited CWD ×
month interactions (Appendix C.2(c)). Over all coleopteran families, Sorenson’s index of
similarity was 0.87 between CWD+ and CWD- treatments. The difference consisted of
four unique families in the CWD+ treatment (Cryptophagidae, Ciidae, Mycetophagidae,
and Throscidae) which are all fungivores, and three families in the CWD– treatment
(Buprestidae, Geotrupide, and Ptinidae), two of which are fungivorous.
Pan traps
Coleoptera abundance in pan traps was significantly greater in association with
ash CWD (1,544 in CWD+ vs. 1,320 in CWD–) and coleopteran family richness and
diversity (Shannon’s and Simpson’s) were also greater in the presence of ash CWD
(Table 3.4a). Similarly, there were temporal differences in coleopteran population
parameters, and there were significant CWD × month interactions for Simpson’s diversity
index. Abundance, richness, and both diversity indices were greatest in June, and
evenness was greatest in May, June, and July (Appendix B.3(a)).
Herbivores, predators and saprophages captured in pan traps were significantly
more abundant in the presence of ash CWD, and the remaining feeding guilds did not
differ (Table 3.4b). Seasonal differences were evident for each feeding guild (Table
30
3.4b). The abundance of fungivores was greatest in June and in August. Herbivores,
saprophages and xylophages were most abundant in June. Predator abundance was
highest in April, May, and June. Xylophages were significantly greater in association
with ash CWD in April (p<0.01) (Appendix C.3(b)).
Of the 46 coleopteran families captured in pan traps, three were significantly
more abundant in association with ash CWD and three were more abundant where ash
CWD was absent (Table 3.4c). Coleopteran abundance differed by month for most taxa,
but only Scolytinae exhibited a CWD × month interaction (Table 3.4c), where abundance
in the CWD+ treatment was greatest in April (Appendix C.3(c)). Over all families,
Sorenson’s index of similarity equaled 0.84 between CWD treatments, with differences
consisting of eight unique families in the CWD+ treatment and five in the CWD–
treatment. Four of the unique families associated with ash CWD were fungivores (Ciidae,
Cryptophagidae, Ptillidae, and Zopheridae), and two unique fungivores (Cupedidae and
Synchroidae) found in the absence of ash CWD.
Discussion
EAB-induced ash mortality causes drastic changes in forest composition and
structure (Gandhi and Herms 2010a), resulting in significant inputs of ash woody
material and with substantial consequences for arthropod associates (Schowalter 2012). I
monitored arthropods in plots with significant downed ash and compared them to plots
lacking downed ash, and demonstrate discernable differences between coleopteran
communities associated with its presence or absence. The comparative approach
evaluating arthropods in the presence or absence of ash coarse woody debris provides a
31
means of estimating potential long-term changes in coleopteran community structure in
the wake of the emerald ash borer invasion.
I found that coleopteran family richness and diversity are associated with
increases in coarse woody debris in two of my three sampling approaches (funnel and pan
traps), and several coleopteran guilds, including fungivores, herbivores, saprophages, and
predators, appear to benefit from the influx of coarse woody debris to the forest floor.
Although not directly associated with the ash coarse woody debris, the appearance of the
parasitic passandrid, Catogenus rufus, in my study is not surprising given its previously
documented association with emerald ash borer invaded forests (Davidson and Rieske
2015). The increases in coarse woody debris associated with EAB-induced ash mortality
create and alter habitats, and local habitat characteristics influence arthropod activity
(Dauber et al. 2005). Thus, these differences in the coleopteran community I document
were anticipated given the varied microhabitats and differing roles occupied by different
feeding guilds. I used the coarser taxonomic resolution of family and guild in my analysis
because ‘taxonomic sufficiency’ recognizes that, within a community, changes at the
species level are often reflected at these coarser taxonomic levels (Ellis 1985, Birkhofer
et al., 2012); I found differences in the coarser taxonomic resolution based on the
presence or absence of ash coarse woody debris. However, even though coleopteran
families are relatively uniform trophically (Hammond 1990, Hammond 1992), the use of
coarser taxonomic identifications in ecological monitoring can be misleading (Longcore
2003), as not all genera in a given family function in the same trophic role.
In my study Sorenson’s index of similarity revealed that 84 – 90% of the
coleopteran community were similar regardless of the presence of ash coarse woody
32
debris, and plots associated with ash coarse woody debris had a similar number of unique
taxa (16) compared to plots with coarse woody debris absent (14). However, when
focusing on fungivores, the number of unique families associated with coarse woody
debris was substantially greater than in plots lacking coarse woody debris (11 vs 4
families). Fungivorous insect abundance is positively correlated with downed woody
material (Vanderwal et al. 2006). The increased abundance of fungivores in my study
suggests a potential functional change that may be occurring as coarse woody debris
volume increases due to EAB-induced ash mortality and all decay classes become
available.
The post-invasion forest plots supported an abundance of Scolytines utilizing the
stressed and standing dead ash, and fungivores utilizing the increasing volume and
variable state of decaying ash coarse woody debris. Bark and ambrosia beetles may play
a role in the initial process of decomposition of stressed and standing dead trees through
gallery construction and reproduction (Iidzuka et al. 2014), where the gallery entrances
can be a starting point for wood decomposition (Lindgren 1990). Their tunneling
activities further influence rates of decomposition by facilitating colonization by
microbes and other organisms, improving aeration, and promoting fragmentation
(Ulyshen 2014), potentially aiding in eventual community recovery (Schowalter 2012).
The tunneling activities of Scolytines can undermine the structural integrity of wood
(Blackman et al. 1924) hastening the fall of emerald ash borer-killed ash trees and
branches, which decay more quickly than standing or suspended wood (Swift et al. 1976).
Following the inputs of ash coarse woody debris, fungivores may then accelerate
33
decomposition of the downed ash resource, thus returning nutrients back to the system
more rapidly.
In my study, a single xylomycetophagous non-native Scolytinae, Xyleborinus
saxeseni (Ratzeburg), represented 89% of the Coleoptera captured in funnel traps (Table
3.6). Xyleborinus saxeseni is globally distributed and was among the first non-native
scolytids documented in North America (Rabaglia et al. 2006). It is also one of the most
damaging and potentially aggressive ambrosia beetles in the tribe Xyleborini in North
America (Rabaglia et al. 2006) feeding on ectosymbiotic fungi growing in wood and on
the wood itself (Deyrup and Atkinson 1987). My results suggest that EAB-induced ash
mortality at these heavily impacted sites has created and modified the forest, creating
optimal habitat and favoring subsequent colonization by Xyleborinus saxeseni. This
secondary invasion by a second non-native insect may be indicative of an ‘invasional
meltdown’ (Simberloff and Von Holle 1999), where each non-native invader enhances
the likelihood and success of subsequent non-native invaders. It’s possible that habitat
modifications by X. saxeseni and its fungal symbionts, through hastened tree fall and
decomposition, may favor the success of other non-native species, including their fungal
associates. If true, the influx of non-natives competing for the same resources as natives
could lead to displacement or local extinction of native insect associates, specifically
fungivores. Further research is needed to assess the impacts of X. saxeseni on these forest
systems following depletion of the ash resources.
My findings have conservation implications. Species richness of ground beetles is
positively correlated with downed woody material on a local scale (Gunnarsson et al.
2004), and 20 m3/ha of downed woody material is suggested to protect litter-dwelling
34
fauna (Kappes et al. 2009). The CWD+ plots contained 17.5 m3/ha of coarse woody
debris with many large diameter snags still standing, suggesting that post EAB-invaded
forests will attain or even surpass the suggested amount of coarse woody debris to
optimize habitat for ground-dwelling arthropods. Coarse woody material decomposes
much more slowly than foliage and fine woody material, creating more resilient habitat
and providing a long term source of nutrients (Harmon et al. 1986, Johnson and Curtis
2001, Greenberg 2002) that can be utilized by a variety of organisms (Hagan and Grove
1999, Åström et al. 2005). The increases in coarse woody debris following EAB
outbreaks could alter forest susceptibility to fire (Jenkins et al. 2008), however mesic
forests in the eastern U.S. are not typically prone to catastrophic fires (Evans 2011). After
evaluating biotic and abiotic risks following emerald ash borer invasion, conservationists
should optimize the amount of coarse woody debris retained to increase arthropod
richness and diversity, and to provide crucial habitat for a variety of wildlife (Evans
2011).
35
Fig. 3.1. Layout of plots, traps, and trap types used to evaluate the arthropod community
associated with ash coarse woody debris in emerald ash borer-impacted forests.
36
Fig. 3.2. Volume (m3/0.1 ac.) of ash coarse woody debris in each decay class (mean
(s.e.)) six years following invasion of emerald ash borer. Means followed by the same
letter are not significantly different at α = 0.05 (F3,29= 9.58; P< 0.01).
a
a
bb
0.00
0.10
0.20
0.30
0.40
0.50
1 2 3 4 5
CWD
Volu
me
/ plo
t (m
3/0.
1 ac
)
Decay Class
Table 3.1. Effects of the presence of coarse woody debris and of season (Fdf/P) on coleopteran a) population parameters, b) feeding
guild abundance, and c) family abundance sampled from funnel traps in EAB invaded forests of north-central Kentucky. Means
followed by the same letter do not significantly differ (P<0.05).
Funnel traps CWD CWD (mean (s.e.)) Month CWD × Month
F1,342/P Present Absent F4,342/P F4,342/P
(a) Population parameters Abundance 2.36/0.13 6.38 (0.53)a 5.56 (0.53)a 90.83/<0.01 0.42/0.79
Richness 16.33/<0.01 6.19 (0.24)a 5.22 (0.24)b 43.33/<0.01 1.56/0.19 Shannon's diversity 11.27/<0.01 1.25 (0.04)a 1.10 (0.04)b 134.15/<0.01 1.00/0.41 Shannon's evenness 2.34/0.13 0.73 (0.03)a 0.70 (0.03)a 97.47/<0.01 2.27/0.07 Simpson's diversity 10.56/<0.01 0.58 (0.03)a 0.49 (0.03)b 77.65/<0.01 2.95/0.03 (b) Feeding guild
Fungivore 15.42/<0.01 3.24 (0.18)a 2.54 (0.18)b 22.3/<0.01 0.66/0.62 Herbivore 8.91/<0.01 3.50 (0.19)a 2.95 (0.19)b 23.2/<0.01 0.11/0.98 Saprophage 8.0/<0.01 2.36 (0.16)a 1.92 (0.16)b 157.8/<0.01 2.06/0.10 Xylophage 0.71/0.40 9.07 (1.06)a 8.17 (1.06)a 114.3/<0.01 0.64/0.63 Predator 3.29/0.07 3.38 (0.18)a 3.06 (0.18)a 17.21/<0.01 0.86/0.49 Parasitoid 0.03/0.86 0.07 (0.05)a 0.08 (0.05)a 7.72/<0.01 0.03/0.99 (c) Families
Aderidae 4.46/0.04 0.07 (0.08)b 0.23 (0.08)a 3.33/0.01 0.74/0.57
37
Table 3.1 (continued)
Funnel traps CWD CWD (mean (s.e.)) Month CWD × Month
F1,342/P Present Absent F4,342/P F4,342/P
Cerylonidae 7.77/<0.01 0.51 (0.10)a 0.24 (0.10)b 19.48/<0.01 1.95/0.11 Ciidae 6.25/0.01 0.28 (0.09)a 0.04 (0.09)b 1.23/0.31 0.36/0.84 Endomychidae 3.95/0.05 0.33 (0.09)a 0.15 (0.09)b 13.75/<0.01 1.06/0.38 Eucnemidae 6.58/0.01 0.47 (0.12)a 0.16 (0.12)b 7.83/<0.01 2.71/0.04 Monotomidae 4.78/0.03 0.15 (0.05)a 0.02 (0.05)b 3.27/0.02 2.26/0.07 Mordellidae 10.36/<0.01 1.42 (0.15)a 0.93 (0.15)b 31.42/<0.01 1.97/0.11 Ptilodactylidae 6.29/0.01 2.26 (0.15)a 1.89 (0.15)b 177.92/<0.01 2.42/0.06 Silphidae 5.99/0.02 0.13 (0.05)a 0.00 (0.05)b 2.36/0.06 2.36/0.06 Staphylinidae 4.03/0.05 3.08 (0.18)a 2.71 (0.18)b 10.92/<0.01 0.30/0.88 Melandryidae 3.13/0.08 0.37 (0.09)a 0.21 (0.09)b 10.16/<0.01 2.19/0.08 Synchroidae 3.10/0.08 0.30 (0.10)a 0.13 (0.10)b 3.30/0.02 0.56/0.69
38
Table 3.2. Effects of the presence of coarse woody debris and of season (Fdf/P) on scolytinae species abundance (S.E.) sampled from
funnel traps in EAB invaded forests of north-central Kentucky in 2015. Means followed by the same letter do not significantly differ
(P<0.05).
Scolytinae Species CWD CWD (s.e.) Month CWD × Month
Funnel traps F1,16/P Present Absent F4,64/P F4,64/P
Xyleborinus saxeseni 0.88/0.36 7.95 (0.82)a 6.86 (0.82)a 112.21/<0.01 0.61/0.66
Ambrosiodmus tachygraphus 0.00/0.96 0.26 (0.05)a 0.26 (0.05)a 60.98/<0.01 0.00/1.00
Euwallacea validus 2.73/0.12 0.56 (0.08)a 0.38 (0.08)a 37.76/<0.01 1.81/0.14
Hypothenemus dissimilis 0.00/1.00 0.02 (0.02)a 0.02 (0.02)a 0.75/0.56 1.25/0.30
Monarthrum fasciatum 0.18/0.68 1.53 (0.12)a 1.46 (0.12)a 229.47/<0.01 0.17/0.96
Monarthrum mali 1.00/0.33 0.02 (0.02)a 0.00 (0.02)a 1.00/0.41 1.00/0.41
Pityophthorus concentralis 1.00/0.33 0.02 (0.02)a 0.00 (0.02)a 1.00/0.41 1.00/0.41
Pseudothysannoes dislocatus 0.39/0.54 0.04 (0.04)a 0.08 (0.04)a 1.09/0.37 1.05/0.39
Xyleborus ferrugineus 0.36/0.55 0.04 (0.03)a 0.02 (0.03)a 3.27/0.02 0.36/0.83
Xyleborus pelliculosus 0.14/0.71 1.33 (0.18)a 1.23 (0.18)a 104.42/<0.01 0.26/0.90
Xylosandrus crassiusculus 1.23/0.28 0.49 (0.11)a 0.66 (0.11)a 10.45/<0.01 0.61/0.66
Xylosandrus germanus 0.86/0.37 0.14 (0.07)a 0.23 (0.07)a 0.77/0.55 0.16/0.96
39
Table 3.2 (continued)
Scolytinae Species CWD CWD (s.e.) Month CWD × Month
Funnel traps F1,16/P Present Absent F4,64/P F4,64/P
Anisandrus sayi 1.55/0.23 0.90 (0.14)a 1.16 (0.14)a 61.87/<0.01 0.59/0.67
40
Table 3.3. Effects of the presence of coarse woody debris and of season (Fdf/P) on coleopteran a) population parameters, b) feeding
guild abundance, and c) family abundance sampled from pitfall traps in EAB invaded forests of north-central Kentucky. Means
followed by the same letter do not significantly differ (P<0.05).
Pitfall traps CWD CWD (s.e) Month CWD × Month
F1,342/P Present Absent F4,342/P F4,342/P
(a) Population
Abundance 4.01/0.05 2.42 (0.13)b 2.68 (0.13)a 14.77/<0.01 1.01/0.41
Richness 0.39/0.53 2.68 (0.15)a 2.77 (0.15)a 41.19/<0.01 0.66/0.62 Shannon's diversity 0.06/0.81 0.72 (0.05)a 0.73 (0.05)a 31.18/<0.01 0.54/0.71 Shannon's evenness 1.23/0.27 0.64 (0.04)a 0.60 (0.04)a 17.84/<0.01 0.32/0.86 Simpson's diversity 0.70/0.41 0.40 (0.03)a 0.42 (0.03)a 23.41/<0.01 1.20/0.32 (b) Feeding guild
Fungivore 7.76/<0.01 3.02 (0.24)b 3.69 (0.24)a 36.76/<0.0 0.92/0.45 Herbivore 0.00/0.97 1.29 (0.16)a 1.30 (0.16)a 3.40/0.01 0.66/0.62 Saprophage 0.08/0.78 0.33 (0.15)a 0.38 (0.15)a 10.02/<0.0 0.35/0.84 Xylophage 0.42/0.52 1.23 (0.15)a 1.13 (0.15)a 36.34/<0.0 0.30/0.88 Predator 0.08/0.78 2.50 (0.17)a 2.55 (0.17)a 14.95/<0.0 0.88/0.48 Parasitoid N/A N/A N/A N/A N/A (c) Families
Carabidae 3.92/0.05 1.54 (0.18)b 1.90 (0.18)a 9.13/<0.01 0.50/0.74 Cryptophagidae 3.18/0.08 0.07 (0.04)a 0.00 (0.04)b 0.53/0.71 0.53/0.71
41
Table 3.3 (continued) Pitfall traps CWD CWD (s.e) Month CWD × Month
F1,342/P Present Absent F4,342/P F4,342/P
Chrysomelidae 7.48/<0.01 0.12 (0.09)b 0.36 (0.09)a 1.49/0.22 2.16/0.08 Elateridae 3.50/0.07 0.17 (0.06)a 0.05 (0.06)b 7.40/<0.01 1.14/0.35 Nitidulidae 8.68/<0.01 2.73 (0.24)b 3.43 (0.24)a 38.26/<0.01 0.77/0.55
42
Table 3.4. Effects of the presence of coarse woody debris and of season (Fdf/P) on coleopteran a) population parameters, b) feeding
guild abundance, and c) family abundance sampled from pan traps in EAB invaded forests of north-central Kentucky. Means followed
by the same letter do not significantly differ (P<0.05).
Pan traps CWD CWD (s.e) Month CWD × Month
F1,342/P Present Absent F4,342/P F4,342/P
(a) Population
Abundance 5.80/0.02 2.73 (0.09)a 2.51 (0.09)b 102.43/ <0.01 0.47/0.76
Richness 5.42/0.02 3.84 (0.19)a 3.41 (0.19)b 107.93/<0.01 0.17/0.95 Shannon's diversity 5.48/0.02 0.97 (0.05)a 0.86 (0.05)b 77.66/<0.01 0.41/0.80 Shannon's evenness 1.56/0.22 0.68 (0.03)a 0.63 (0.03)a 34.16/<0.01 0.58/0.68 Simpson's diversity 8.34/<0.01 0.49 (0.03)a 0.39 (0.03)b 36.49/<0.01 3.56/0.01 (b) Feeding guild
Fungivore 0.74/0.64 2.27 (0.17)a 2.42 (0.17)a 20.76/<0.01 0.84/0.51 Herbivore 5.56/0.02 3.43 (0.20)a 2.97 (0.20)b 89.67/<0.01 1.24/0.30 Saprophage 0.01/0.91 1.10 (0.12)a 1.11 (0.12)a 82.61/<0.01 0.33/0.86 Xylophage 7.17/0.01 1.23 (0.15)a 0.83 (0.15)b 29.57/<0.01 2.93/0.03 Predator 4.38/0.04 2.14 (0.13)a 1.86 (0.13)b 41.44/<0.01 0.26/0.90 Parasitoid N/A N/A N/A N/A N/A (c) Families
Chrysomelidae 13.40/<0.01 2.02 (0.15)a 1.46 (0.15)b 71.33/<0.01 2.24/0.07
43
Table 3.4 (continued)
Pan traps CWD CWD (s.e) Month CWD × Month
F1,342/P Present Absent F4,342/P F4,342/P
Cupedidae 3.21/0.08 0.00 (0.04)b 0.07 (0.04)a 1.43/0.23 1.43/0.23 Phalacridae 3.21/0.08 0.07 (0.04)a 0.00 (0.04)b 1.43/0.23 1.43/0.23 Ptinidae 2.96/0.09 0.17 (0.09)b 0.33 (0.09)a 8.75/<0.01 1.14/0.35 Scolytinae 6.87/0.01 0.74 (0.13)a 0.40 (0.13)b 19.63/<0.01 4.57/<0.01 Throscidae 2.78/0.10 0.12 (0.11)b 0.31 (0.11)a 4.27/<0.01 0.62/0.65
44
45
APPENDICES
46
APPENDIX A
Trophic guild designations
Coleopteran family abundance relative to ash canopy decline at five forested sites in
north central Kentucky with trophic guild designations including; herbivores (H),
fungivores (F), predators (P), saprophages (S), xylophages (X), and parasitoids (Pa).
Coleopteran Families
Trophic Guilds
Abundance Fayette Spencer Shelby Anderson Henry Absolute
Elateridae H 205 345 678 353 240 1,821 Chrysomelidae H 127 176 272 56 55 686 Curculionidae H 81 127 154 99 113 574 Tenebrionidae H 94 83 142 54 154 527 Mordellidae H 48 103 148 75 59 433 Scarabaeidae H 20 24 20 23 23 110 Phalacridae H 2 5 26 6 12 51 Attelabidae H 0 0 2 0 3 5 Latridiidae F 141 33 274 230 340 1,018 Corylophidae F 21 2 73 41 94 231 Ptinidae F 16 47 38 36 13 150 Eucnemidae F 16 50 33 39 8 146 Erotylidae F 14 14 8 16 17 69 Mycetophagidae F 22 5 16 6 10 59 Tetratomidae F 3 12 7 21 15 58 Nitidulidae F 7 13 11 11 13 55 Cerylonidae F 15 4 8 13 7 47 Zopheridae F 6 10 5 13 5 39 Silvanidae F 1 22 1 6 7 37 Melandryidae F 5 11 10 6 4 36 Synchroidae F 4 4 6 9 9 32 Endomychidae F 7 1 6 4 4 22 Leiodidae F 5 2 3 8 4 22 Cryptophagidae F 0 1 4 3 0 8 Laemophloeidae F 3 1 1 2 1 8 Anthribidae F 4 1 0 1 0 6 Cucujidae F 0 0 1 1 0 2 Pyrochoidae F 0 0 1 0 1 2 Sphindidae F 0 0 1 1 0 2 Throscidae F 0 1 0 0 1 2 Salpingidae F 1 0 0 0 0 1
47
Staphylinidae P 225 224 356 443 192 1,440 Histeridae P 188 316 141 204 136 985 Trogossitidae P 27 42 46 43 70 228 Carabidae P 16 20 63 43 34 176 Cleridae P 7 27 31 31 48 144 Lampyridae P 3 14 14 13 4 48 Coccinellidae P 5 7 4 0 2 18 Melyridae P 1 0 1 0 4 6 Cantharidae P 0 2 1 0 0 3 Hydrophilidae P 0 1 0 0 0 1 Lycidae P 0 0 0 1 0 1 Ptilodactylidae S 139 131 480 266 40 1,056 Dermestidae S 7 26 1 6 7 47 Monotomidae S 2 6 0 0 0 8 Scirtidae S 0 1 0 3 0 4 Hybosoridae S 2 0 0 1 0 3 Silphidae S 0 Scolytinae X 168 465 107 117 134 991 Scraptiidae X 1 1 8 24 53 87 Cerambycidae X 6 13 12 19 24 74 Bostrichidae X 1 5 2 0 3 11 Buprestidae X 0 0 2 2 5 9 Lucanidae X 0 0 0 1 0 1 Lymexylidae X 0 0 0 1 0 1 Passandridae Pa 21 13 14 16 14 78 Rhipiceridae Pa 1 0 0 1 2 4 Bothrideridae Pa 0 3 0 0 0 3 Unidentified --- 33 22 9 21 15 100 Total 1,721 2,436 3,241 2,389 1,999 11,786
APPENDIX B
Temporal data by month
Temporal effects on the coleopteran community (mean (s.e.)) for coleopteran a) population parameters, b) feeding guild abundance,
and c) family abundance (for families where CWD treatment interaction α=0.1) sampled from all trap types in EAB invaded forests of
north-central Kentucky. Means followed by the same letter do not significantly differ (P<0.05).
Month
April May June July August
(I) FUNNEL TRAPS (a) Population parameters Abundance 15.9 (0.6)a 3.7 (0.6)bc 4.9 (0.6)b 3.3 (0.6)bc 2.0 (0.6)c Richness 5.7 (0.3)b 5.6 (0.3)b 8.2 (0.3)a 5.8 (0.3)b 3.2 (0.3)c Shannon's diversity 0.3 (0.1)d 1.3 (0.1)b 1.7 (0.1)a 1.5 (0.1)a 1.0 (0.3)c Simpson's diversity 0.1 (0.0)d 0.6 (0.0)b 0.8 (0.0)a 0.8 (0.0)ab 0.4 (0.0)c Shannon's evenness 0.2 (0.0)b 0.8 (0.0)a 0.8 (0.0)a 0.9 (0.0)a 0.8 (0.0)a (b) Feeding guild Fungivore 4.5 (0.2)a 2.8 (0.2)b 2.6 (0.2)b 2.3 (0.2)b 2.3 (0.2)b Herbivore 2.3 (0.2)bc 3.0 (0.2)b 4.5 (0.2)a 4.0 (0.2)a 2.2 (0.2)c Saprophage 0.2 (0.2)d 1.8 (0.2)c 5.4 (0.2)a 2.9 (0.2)b 0.3 (0.2)d Xylophage 31.1 (1.2)a 4.7 (1.2)b 4.7 (1.2)b 1.8 (1.2)b 0.9 (1.2)b Predator 4.2 (0.2)a 3.3 (0.2)b 3.5 (0.2)ab 2.9 (0.2)b 2.1 (0.2)c Parasitoid 0.0 (0.1)b 0.0 (0.1)b 0.4 (0.1)a 0.0 (0.1)b 0.0 (0.1)b
48
(c) Families Aderidae 0.0 (0.1)b 0.1 (0.1)ab 0.2 (0.1)ab 0.4 (0.1)a 0.0 (0.1)b Cerylonidae 1.2 (0.1)a 0.3 (0.1)b 0.4 (0.1)b 0.0 (0.1)b 0.0 (0.1)b Ciidae 0.2 (0.1)a 0.1 (0.1)a 0.1 (0.1)a 0.3 (0.1)a 0.1 (0.1)a Endomychidae 0.9 (0.1)a 0.1 (0.1)b 0.1 (0.1)b 0.1 (0.1)b 0.0 (0.1)b Eucnemidae 0.0 (0.1)b 0.4 (0.1)ab 0.9 (0.1)a 0.2 (0.1)b 0.1 (0.1)b Monotomidae 0.2 (0.1)a 0.0 (0.1)a 0.2 (0.1)a 0.0 (0.1)a 0.0 (0.1)a Mordellidae 0.0 (0.2)c 0.4 (0.2)b 2.1 (0.2)a 2.0 (0.2)a 1.5 (0.2)a Ptilodactylidae 0.0 (0.2)d 1.8 (0.2)c 5.4 (0.2)a 2.9 (0.2)b 0.3 (0.2)d Silphidae 0.0 (0.1)a 0.0 (0.1)a 0.1 (0.1)a 0.2 (0.1)a 0.0 (0.1)a Staphylinidae 3.7 (0.2)a 3.1 (0.2)ab 3.1 (0.2)ab 2.7 (0.2)b 1.9 (0.2)c Melandryidae 0.0 (0.1)c 0.5 (0.1)ab 0.0 (0.1)c 0.2 (0.1)bc 0.8 (0.1)a Synchroidae 0.0 (0.1)b 0.1 (0.1)ab 0.4 (0.1)a 0.2 (0.1)ab 0.4 (0.1)ab (II) PITFALL TRAPS (a) Population parameters Abundance 1.9 (0.1)c 2.4 (0.1)b 3.3 (0.1)a 2.4 (0.1)b 2.8 (0.1)b Richness 1.6 (0.2)c 2.8 (0.2)b 4.5 (0.2)a 2.4 (0.2)b 2.4 (0.2)b Shannon's diversity 0.4 (0.1)c 0.8 (0.1)b 1.2 (0.1)a 0.6 (0.1)b 0.6 (0.1)b Simpson's diversity 0.2 (0.0)c 0.4 (0.0)b 0.7 (0.0)a 0.4 (0.0)b 0.3 (0.0)bc Shannon's evenness 0.4 (0.0)d 0.7 (0.0)ab 0.8 (0.0)a 0.6 (0.0)c 0.6 (0.0)bc (b) Feeding guild Fungivore 0.7 (0.3)c 3.0 (0.3)b 4.6 (0.3)a 3.8 (0.3)ab 4.6 (0.3)a Herbivore 1.0 (0.2)b 1.0 (0.2)ab 1.6 (0.2)ab 1.3 (0.2)ab 1.7 (0.2)a Saprophage 0.0 (0.2)b 0.3 (0.2)b 1.3 (0.2)a 0.2 (0.2)b 0.0 (0.2)b Xylophage 2.7 (0.2)a 0.9 (0.2)c 1.7 (0.2)b 0.3 (0.2)c 0.4 (0.2)c Predator 1.8 (0.2)c 2.9 (0.2)ab 3.6 (0.2)a 2.0 (0.2)c 2.2 (0.2)bc (c) Families
49
Carabidae 0.8 (0.2)c 1.8 (0.2)ab 2.5 (0.2)a 1.6 (0.2)b 1.8 (0.2)ab Cryptophagidae 0.1 (0.0)a 0.1 (0.0)a 0.1 (0.0)a 0.0 (0.0)a 0.0 (0.0)a Chrysomelidae 0.2 (0.1)a 0.1 (0.1)a 0.4 (0.1)a 0.2 (0.1)a 0.2 (0.1)a Elateridae 0.0 (0.1)b 0.1 (0.1)b 0.5 (0.1)a 0.1 (0.1)b 0.0 (0.1)b Nitidulidae 0.5 (0.3)c 2.4 (0.3)b 4.2 (0.3)a 3.7 (0.3)a 4.5 (0.3)a (III) PAN TRAPS (a) Population parameters Abundance 2.2 (0.1)bc 2.0 (0.1)c 4.4 (0.1)a 2.6 (0.1)b 1.9 (0.1)c Richness 2.0 (0.2)d 2.9 (0.2)c 7.3 (0.2)a 3.9 (0.2)b 2.1 (0.2)d Shannon's diversity 0.4 (0.1)c 0.9 (0.1)b 1.6 (0.1)a 1.0 (0.1)b 0.6 (0.1)c Simpson's diversity 0.2 (0.0)c 0.4 (0.0)b 0.8 (0.0)a 0.5 (0.0)b 0.3 (0.0)b Shannon's evenness 0.3 (0.0)c 0.8 (0.0)a 0.8 (0.0)a 0.8 (0.0)a 0.6 (0.0)b (b) Feeding guild Fungivore 1.0 (0.2)c 2.3 (0.2)b 3.3 (0.2)a 2.3 (0.2)b 2.9 (0.2)ab Herbivore 2.1 (0.2)c 1.5 (0.2)c 6.5 (0.2)a 4.0 (0.2)b 2.0 (0.2)c Saprophage 0.1 (0.1)d 0.7 (0.1)c 3.1 (0.1)a 1.3 (0.1)b 0.4 (0.1)cd Xylophage 2.0 (0.2)a 0.5 (0.2)b 2.0 (0.2)a 0.5 (0.2)b 0.1 (0.2)b Predator 2.8 (0.2)a 2.4 (0.2)a 2.8 (0.2)a 1.5 (0.2)b 0.6 (0.2)c (c) Families Chrysomelidae 1.1 (0.2)c 0.4 (0.2)d 4.1 (0.2)a 2.1 (0.2)b 1.1 (0.2)c Cupedidae 0.0 (0.0)a 0.0 (0.0)a 0.1 (0.0)a 0.1 (0.0)a 0.0 (0.0)a Phalacridae 0.1 (0.0)a 0.1 (0.0)a 0.0 (0.0)a 0.0 (0.0)a 0.0 (0.0)a Ptinidae 0.0 (0.1)b 0.1 (0.1)b 0.7 (0.1)a 0.4 (0.1)ab 0.1 (0.1)b Scolytinae 1.7 (0.1)a 0.2 (0.1)b 0.6 (0.1)b 0.3 (0.1)b 0.1 (0.1)b Throscidae 0.0 (0.1)b 0.5 (0.1)a 0.5 (0.1)ab 0.1 (0.1)ab 0.0 (0.1)b (IV) Scolytines Xyleborinus saxeseni 29.35 (1.17)a 4.13 (1.17)b 2.83 (1.17)b 0.30 (1.17)b 0.41 (1.17)b
50
Ambrosiodmus tachygraphus 1.29 (0.07)a 0.00 (0.07))b 0.00 (0.07)b 0.00 (0.07)b 0.00 (0.07)b Euwallacea validus 1.70 (0.12)a 0.17 (0.12)bc 0.47 (0.12)b 0.00 (0.12)c 0.00 (0.12)c Hypothenemus dissimilis 0.06 (0.04)a 0.00 (0.04)a 0.00 (0.04)a 0.00 (0.04)a 0.06 (0.04)a Monarthrum fasciatum 6.72 (0.19)a 0.59 (0.19)b 0.11 (0.19)b 0.06 (0.19)b 0.00 (0.19)b Monarthrum mali 0.06 (0.02)a 0.00 (0.02)a 0.00 (0.02)a 0.00 (0.02)a 0.00 (0.02)a Pityophthorus concentralis 0.06 (0.02)a 0.00 (0.02)a 0.00 (0.02)a 0.00 (0.02)a 0.00 (0.02)a Pseudothysannoes dislocatus 0.00 (0.06)a 0.11 (0.06)a 0.13 (0.06)a 0.06 (0.06)a 0.00 (0.06)a Xyleborus ferrugineus 0.00 (0.04)b 0.00 (0.04)b 0.17 (0.04)a 0.00 (0.04)b 0.00 (0.04)b Xyleborus pelliculosus 6.33 (0.28)a 0.00 (0.28)b 0.00 (0.28)b 0.00 (0.28)b 0.06 (0.28)b Xylosandrus crassiusculus 0.64 (0.14)bc 0.69 (0.14)ab 1.14 (0.14)a 0.17 (0.14)c 0.22 (0.14)c Xylosandrus germanus 0.17 (0.10)a 0.06 (0.10)a 0.25 (0.10)a 0.28 (0.10)a 0.19 (0.10)a Anisandrus sayi 0.25 (0.17)c 0.81 (0.17)b 3.01 (0.17)a 1.11 (0.17)b 0.00 (0.17)c
51
APPENDIX C
CWD × Month treatment interactions
Effects of the presence of coarse woody debris (CWD+ mean (s.e.); CWD- mean (s.e)) by month on coleopteran a) population
parameters, b) feeding guild abundance, and c) family abundance (for families where CWD treatment interaction α=0.1) sampled from
all trap types in EAB invaded forests of north-central Kentucky. Asterisks following a value indicate a significant CWD × Month
interaction for that parameter.
Month
April May June July August
(I) FUNNEL TRAPS (a) Population parameters Abundance 17.0(0.8); 14.8(0.8) 3.9(0.8); 3.5(0.8) 5.2(0.8); 4.5(0.8) 3.4(0.8); 3.1(0.8) 2.3(0.8); 1.8(0.8) Richness 5.8(0.4); 5.6(0.4) 6.2(0.4); 4.9(0.4) 9.2(0.4); 7.3(0.4)* 6.1(0.4); 5.5(0.4) 3.7(0.4); 2.9(0.4) Shannon's diversity 0.3(0.1); 0.3(0.1) 1.4(0.1); 1.2(0.1) 1.8(0.1); 1.6(0.1) 1.6(0.1); 1.5(0.1) 1.2(0.1); 0.9(0.1) Simpson's diversity 0.2(0.0); 0.2(0.0) 0.8(0.0); 0.8(0.0) 0.8(0.0); 0.8(0.0) 0.9(0.0); 0.9(0.0) 0.9(0.0); 0.9(0.0) Shannon's evenness 0.1(0.1); 0.1(0.1) 0.7(0.1); 0.6(0.1) 0.8(0.1); 0.8(0.1) 0.8(0.1); 0.7(0.1) 0.5(0.1); 0.2(0.1)* (b) Feeding guild Fungivore 5.0(0.3); 4.1(0.3) 3.1(0.3); 2.5(0.3) 3.1(0.3); 2.0(0.4) 2.4(0.3); 2.2(0.3) 2.6(0.3); 1.9(0.3) Herbivore 2.7(0.3); 2.0(0.3) 3.3(0.3); 2.8(0.3) 4.8(0.3); 4.2(0.3) 4.2(0.3); 3.8(0.3) 2.5(0.3); 2.0(0.3) Saprophage 0.3(0.3); 0.1(0.3) 1.8(0.3); 1.8(0.3) 6.2(0.3); 4.8(0.3)* 3.0(0.3); 2.9(0.3) 0.5(0.3); 0.0(0.3) Xylophage 33.2(1.7); 29.0(1.7) 5.0(1.7); 4.4(1.7) 4.7(1.7); 4.8(1.7) 1.6(1.7); 1.9(1.7) 0.9(1.7); 0.8(1.7) Predator 4.2(0.3); 4.4(0.3) 3.4(0.3); 3.2(0.3) 3.8(0.3); 3.3(0.3) 3.2(0.3); 2.5(0.3) 2.3(0.3); 1.9(0.3)
52
Parasitoid 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) 0.3(0.1); 0.4(0.1) 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) (c) Families Aderidae 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.3(0.1) 0.1(0.1); 0.4(0.1) 0.2(0.1); 0.5(0.1) 0.0(0.1); 0.0(0.1) Cerylonidae 1.3(0.2); 1.1(0.2) 0.6(0.2); 0.0(0.2) 0.7(0.2); 0.1(0.2) 0.0(0.2); 0.0(0.2) 0.0(0.2); 0.0(0.2) Ciidae 0.3(0.1); 0.1(0.1) 0.2(0.1); 0.0(0.1) 0.1(0.1); 0.0(0.1) 0.5(0.1); 0.1(0.1) 0.2(0.1); 0.0(0.1) Endomychidae 1.2(0.1); 0.7(0.1) 0.2(0.1); 0.1(0.1) 0.2(0.1); 0.0(0.1) 0.1(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) Eucnemidae 0.0(0.2); 0.0(0.2) 0.7(0.2); 0.1(0.2) 1.4(0.2); 0.5(0.2)* 0.2(0.2); 0.1(0.2) 0.0(0.2); 0.1(0.2) Monotomidae 0.3(0.1); 0.1(0.1) 0.0(0.1); 0.0(0.1) 0.4(0.1); 0.0(0.1)* 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) Mordellidae 0.0(0.2); 0.0(0.2) 0.3(0.2); 0.4(0.2) 2.5(0.2); 1.7(0.2) 2.3(0.2); 1.6(0.2) 1.9(0.2); 1.0(0.2) Ptilodactylidae 0.0(0.2); 0.0(0.2) 1.8(0.2); 1.8(0.2) 6.0(0.2); 4.8(0.2)* 3.0(0.2); 2.9(0.2) 0.5(0.2); 0.0(0.2) Silphidae 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) 0.3(0.1); 0.0(0.1) 0.4(0.1); 0.0(0.1)* 0.0(0.1); 0.0(0.1) Staphylinidae 3.8(0.3); 3.6(0.3) 3.2(0.3); 3.0(0.3) 3.3(0.3); 3.0(0.3) 3.1(0.3); 2.3(0.3) 2.0(0.3); 1.7(0.3) Melandryidae 0.0(0.2); 0.0(0.2) 0.7(0.2); 0.3(0.2) 0.0(0.2); 0.0(0.2) 0.1(0.2); 0.3(0.2) 1.1(0.2); 0.5(0.2) Synchroidae 0.0(0.2); 0.0(0.2) 0.1(0.2); 0.0(0.2) 0.7(0.2); 0.2(0.2) 0.3(0.2); 0.1(0.2) 0.4(0.2); 0.3(0.2) (II) PITFALL TRAPS (a) Population parameters Abundance 2.0(0.2); 1.8(0.2) 2.2(0.2); 2.6(0.2) 3.3(0.2); 3.4(0.2) 2.2(0.2); 2.6(0.2) 2.5(0.2); 3.0(0.2) Richness 1.6(0.2); 1.5(0.2) 2.6(0.2); 3.0(0.2) 4.6(0.2); 4.4(0.2) 2.3(0.2); 2.4(0.2) 2.3(0.2); 2.5(0.2) Shannon's diversity 0.4(0.1); 0.4(0.1) 0.8(0.1); 0.9(0.1) 1.2(0.1); 1.2(0.1) 0.6(0.1); 0.6(0.1) 0.6(0.1); 0.6(0.1) Simpson's diversity 0.4(0.1); 0.3(0.1) 0.7(0.1); 0.7(0.1) 0.8(0.1); 0.8(0.1) 0.6(0.1); 0.5(0.1) 0.6(0.1); 0.6(0.1) Shannon's evenness 0.2(0.1); 0.2(0.1) 0.4(0.1); 0.5(0.1) 0.7(0.1); 0.7(0.1) 0.4(0.1); 0.4(0.1) 0.3(0.1); 0.3(0.1) (b) Feeding guild Fungivore 0.7(0.4); 0.7(0.4) 2.6(0.4); 3.4(0.4) 4.4(0.4); 4.8(0.4) 3.3(0.4); 4.4(0.4) 4.0(0.4); 5.2(0.4) Herbivore 1.1(0.3); 0.8(0.3) 1.0(0.3); 0.9(0.3) 1.4(0.3); 1.7(0.3) 1.2(0.3); 1.5(0.3) 1.7(0.3); 1.6(0.3) Saprophage 0.0(0.2); 0.0(0.2) 0.2(0.2); 0.3(0.2) 1.1(0.2); 1.4(0.2) 0.3(0.2); 0.1(0.2) 0.0(0.2); 0.0(0.2) Xylophage 2.9(0.2); 2.6(0.2) 0.8(0.2); 0.9(0.2) 1.8(0.2); 1.5(0.2) 0.3(0.2); 0.2(0.2) 0.3(0.2); 0.4(0.2) Predator 1.9(0.3); 1.8(0.3) 2.7(0.3); 3.2(0.3) 3.9(0.3); 3.4(0.3) 2.0(0.3); 2.1(0.3) 2.1(0.3); 2.3(0.3)
53
(c) Families Carabidae 0.6(0.3); 1.0(0.3) 1.5(0.3); 2.2(0.3) 2.5(0.3); 2.5(0.3) 1.5(0.3); 1.8(0.3) 1.7(0.3); 2.0(0.3) Cryptophagidae 0.1(0.1); 0.0(0.1) 0.1(0.1); 0.0(0.1) 0.1(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) Chrysomelidae 0.0(0.1); 0.4(0.1) 0.0(0.1); 0.2(0.1) 0.2(0.1); 0.7(0.1) 0.1(0.1); 0.4(0.1) 0.3(0.1); 0.1(0.1) Elateridae 0.0(0.1); 0.0(0.1) 0.1(0.1); 0.0(0.1) 0.6(0.1); 0.3(0.1) 0.1(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) Nitidulidae 0.5(0.4); 0.5(0.4) 2.1(0.4); 2.8(0.4) 4.0(0.4); 4.5(0.4) 3.2(0.4); 4.2(0.4) 3.9(0.4); 5.1(0.4) (III) PAN TRAPS (a) Population parameters Abundance 2.3(0.1); 2.1(0.1) 2.1(0.1); 1.8(0.1) 4.6(0.1); 4.2(0.1) 2.7(0.1); 2.5(0.1) 1.9(0.1); 1.9(0.1) Richness 2.1(0.3); 1.9(0.3) 3.2(0.3); 2.6(0.3) 7.6(0.3); 7.0(0.3) 4.1(0.3); 3.6(0.3) 2.3(0.3); 1.9(0.3) Shannon's diversity 0.5(0.1); 0.4(0.1) 1.0(0.1); 0.8(0.1) 1.7(0.1); 1.6(0.1) 1.1(0.1); 1.0(0.1) 0.7(0.1); 0.5(0.1) Simpson's diversity 0.3(0.1); 0.3(0.1) 0.8(0.1); 0.7(0.1) 0.8(0.1); 0.9(0.1) 0.8(0.1); 0.7(0.1) 0.6(0.1); 0.6(0.1) Shannon's evenness 0.2(0.1); 0.2(0.1) 0.5(0.1); 0.2(0.1)* 0.8(0.1); 0.8(0.1) 0.5(0.1); 0.5(0.1) 0.4(0.1); 0.3(0.1) (b) Feeding guild Fungivore 0.8(0.3); 1.1(0.3) 2.5(0.3); 2.1(0.3) 3.3(0.3); 3.3(0.3) 2.1(0.3); 2.4(0.3) 2.6(0.3); 3.1(0.3) Herbivore 2.0(0.3); 2.2(0.3) 1.7(0.3); 1.3(0.3) 6.9(0.3); 6.0(0.3) 4.2(0.3); 3.8(0.3) 2.5(0.3); 1.5(0.3) Saprophage 0.2(0.3); 0.0(0.3) 0.6(0.3); 0.8(0.3) 3.1(0.3); 3.1(0.3) 1.3(0.3); 1.2(0.3) 0.3(0.3); 0.5(0.3) Xylophage 2.6(0.2); 1.4(0.2)* 0.8(0.2); 0.3(0.2) 2.3(0.2); 1.7(0.2) 0.5(0.2); 0.5(0.2) 0.0(0.2); 0.2(0.2) Predator 3.0(0.2); 2.7(0.2) 2.6(0.2); 2.2(0.2) 2.8(0.2); 2.7(0.2) 1.7(0.2); 1.2(0.2) 0.7(0.2); 0.5(0.2) (c) Families Chrysomelidae 0.9(0.2); 1.2(0.2) 0.6(0.2); 0.1(0.2) 4.6(0.2); 3.5(0.2) 2.6(0.2); 1.7(0.2) 1.4(0.2); 0.8(0.2) Cupedidae 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.1(0.1) 0.0(0.1); 0.2(0.1) 0.0(0.1); 0.0(0.1) Phalacridae 0.1(0.1); 0.0(0.1) 0.2(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.0(0.1) Ptinidae 0.0(0.1); 0.0(0.1) 0.0(0.1); 0.1(0.1) 0.8(0.1); 0.7(0.1) 0.1(0.1); 0.6(0.1) 0.0(0.1); 0.2(0.1) Scolytinae 2.4(0.2); 1.0(0.2)* 0.3(0.2); 0.1(0.2) 0.8(0.2); 0.4(0.2) 0.2(0.2); 0.3(0.2) 0.0(0.2); 0.2(0.2) Throscidae 0.0(0.2); 0.0(0.2) 0.3(0.2); 0.7(0.2) 0.3(0.2); 0.7(0.2) 0.0(0.2); 0.2(0.2) 0.0(0.2); 0.0(0.2)
54
55
APPENDIX D
Scolytine abundance and origin
Abundance of scolytine species captured in funnel traps in 2015 for CWD+ and CWD-
treatments. Known origins also listed.
Scolytinae Species CWD + CWD - Origin
Xyleborinus saxeseni 10,404 7,615 Non-native
Ambrosiodmus tachygraphus 20 18 Native
Euwallacea validus 55 24 Non-native
Hypothenemus dissimilis 1 1 Non-native
Monarthrum fasciatum 450 424 Native
Monarthrum mali 1 0 Uncertain
Pityophthorus concentralis 1 0 Uncertain
Pseudothysannoes dislocatus 2 4 Uncertain
Xyleborus ferrugineus 2 1 Native
Xyleborus pelliculosus 440 395 Non-native
Xylosandrus crassiusculus 30 39 Non-native
Xylosandrus germanus 7 11 Non-native
Anisandrus sayi 103 142 Native
56
REFERENCES
Åström, M., M. Dynesius, K. Hylander, and C. Nilsson. 2005. Effects of slash harvest
on bryophytes and vascular plants in southern boreal forest clear‐cuts. J. Appl.
Ecol. 42: 1194–1202.
Aukema, J.E., B. Leung, K. Kovacs, C. Chivers, K.O. Britton, J. Englin, S.J.
Frankel, R.G. Haight, T.P. Holmes, and A.M. Liebhold. 2011. Economic
impacts of non-native forest insects in the continental United States. PLoS One. 6:
e24587.
Baker, James R., James LaBonte, Thomas Atkinson & Stephen Bambara. 2009. An
Identification Tool For Bark Beetles of the Southeastern United States. Lucid® v.
3.4.1, December, 2009, Latest update [month/year] North Carolina State
University, Raleigh, NC. 27695.
Bauer, L. S., H. Liu, R. A. Haack, T. R. Petrice, and D. L. Miller. 2004. Natural
enemies of emerald ash borer in southeastern Michigan, pp. 33–34. In V. Mastro,
R. Reardon (comps.), Proceedings, Emerald Ash Borer Research and Technology
Development Meeting, 30 September–1 October 2003, Port Huron, MI. U.S.
Forest Service, Forest Health Technology Enterprise Team, Morgantown, WV.
Birkhofer, K., Bezemer, T., Hedlund, K., Setälä, H., 2012. Community composition of
soil organisms under different wheat-farming systems. In: Cheeke, T., Coleman,
D., Wall, D. (Eds.), Microbial Ecology in Sustainable Agroecosystems. CRC
Press, pp. 89–111. doi:10.1201/b12339-6.
57
Blackman, M.W., and H.H. Stage. 1924. On the succession of insects living in the bark
and wood of dying, dead and decaying hickory. N.Y. State Coll For. Tech. Publ.
17: 3–269.
Bouget, C., H. Brustel, A. Brin, and L. Valladares. 2009. Evaluation of window flight
traps for effectiveness at monitoring dead wood‐associated beetles: the effect of
ethanol lure under contrasting environmental conditions. Agric. For. Entomol. 11:
143–152.
Breshears, D.D., N.S. Cobb, P.M. Rich, K.P. Price, C.D. Allen, R.G. Balice, W.H.
Romme, J.H. Kastens, M.L. Floyd, and J. Belnap. 2005. Regional vegetation
die-off in response to global-change-type drought. Proc. Natl. Acad. Sci. USA
102: 15144–15148.
Brown, M., T. Black, Z. Nesic, V. Foord, D. Spittlehouse, A. Fredeen, N. Grant, P.
Burton, and J. Trofymow. 2010. Impact of mountain pine beetle on the net
ecosystem production of lodgepole pine stands in British Columbia. Agric. For.
Meteorol. 150: 254–264.
BugGuide. 2017. Order Coleoptera: Beetles. http://bugguide.net/node/view/60/tree
(Accessed 01 April. 2017).
Byers, J.E., S. Reichard, J.M. Randall, I.M. Parker, C.S. Smith, W.M. Lonsdale,
I.A. Atkinson, T.R. Seastedt, M. Williamson, and E. Chornesky. 2002.
Directing research to reduce the impacts of nonindigenous species. Conserv. Biol.
16: 630–640.
Campbell, J.J. 1989. Historical evidence of forest composition in the Bluegrass Region
of Kentucky, pp. 231–246 in G. Rink and C. Budelsky (eds.), Proceedings,
58
Seventh Central Hardwood Forest Conference, 5-8 March 1989, Carbondale, IL.
General Technical Report, NC-135. St. Paul, MN: U.S. Department of
Agriculture, Forest Service, North Central Forest Experiment Station.
Cappaert, D.D., D.G. McCullough, T.M. Poland, and N.W. Siegert. 2005. Emerald
ash borer in North America: a research and regulatory challenge. Am. Entomol.
51: 152–165.
Coleman, T.W., S.R. Clarke, J.R. Meeker, and L.K. Rieske. 2008. Forest composition
following overstory mortality from southern pine beetle and associated
treatments. Can. J. For. Res. 38: 1406–1418.
Dauber, J., T. Purtauf, A. Allspach, J. Frisch, K. Voigtländer, and V. Wolters. 2005.
Local vs. landscape controls on diversity: a test using surface‐dwelling soil
macroinvertebrates of differing mobility. Global Ecol. Biogeogr. 14: 213–221.
Davidson, W., and L.K. Rieske. 2015. Native parasitoid response to emerald ash borer
(Coleoptera: Buprestidae) and ash decline in recently invaded forests of the
central United States. Ann. Entomol. Soc. Am. 108: 777-784.
Deyrup M, Atkinson TH. 1987. Comparative biology of temperate and subtropical bark
and ambrosia beetles (Coleoptera: Scolytidae, Platypodidae) in Indiana and
Florida. The Great Lakes Entomologist 20: 59-66.
Duan, J.J., L.S. Bauer, K.J. Abell, M.D. Ulyshen, and R.G. Van Driesche. 2015.
Population dynamics of an invasive forest insect and associated natural enemies
in the aftermath of invasion: implications for biological control. J. Appl. Ecol. 52:
1246-1254.
59
Ehrenfeld, J.G. 2010. Ecosystem consequences of biological invasions. Annu. Rev.
Ecol. Syst. 41: 59–80.
Ellis, D. 1985. Taxonomic sufficiency in pollution assessment. Mar. Pollut. Bull. 16: 459.
Evans, A.M. 2011. Ecology of dead wood in the Southeast. Report to the Forest Guild,
Santa Fe, NM. 37 pp.
Evans, A.V. 2014. Beetles of Eastern North America. Princeton University Press,
Princeton, NJ. 560 pp.
Flower, C.E., K.S. Knight, J. Rebbeck, and M.A. Gonzalez-Meler. 2013. The
relationship between the emerald ash borer (Agrilus planipennis) and ash
(Fraxinus spp.) tree decline: using visual canopy condition assessments and leaf
isotope measurements to assess pest damage. For. Ecol. Manage. 303: 143–147.
Gandhi, K.J.K., and D.A. Herms. 2010a. Direct and indirect effects of alien insect
herbivores on ecological processes and interactions in forests of eastern North
America. Biol. Invasions. 12: 389–405.
Gandhi, K.J.K., and D.A. Herms. 2010b. North American arthropods at risk due to
widespread fraxinus mortality caused by the alien emerald ash borer. Biol.
Invasions. 12: 1839–1846.
Greenberg, C.H. 2002. Response of white-footed mice (Peromyscus leucopus) to coarse
woody debris and microsite use in southern Appalachian treefall gaps. For. Ecol.
Manage. 164: 57–66.
Gunnarsson, B., K. Nittérus, and P. Wirdenäs. 2004. Effects of logging residue
removal on ground-active beetles in temperate forests. For. Ecol. Manage. 201:
229–239.
60
Haack, R.A., E. Jendak, L. Houping, K.R. Marchant, T.R. Petrice, T.M. Poland,
and H. Ye. 2002. The emerald ash borer: a new exotic pest in North America.
Newsletter of the Michigan Entomological Society. 47: 1–5.
Hagan, J.M., and S.L. Grove. 1999. Coarse woody debris: humans and nature
competing for trees. J. For. 97: 6–11.
Hammond, P. M. 1990. Insect abundance and diversity in the Dumoga-Bone National
Park, N. Sulawesi, with special reference to the beetle fauna of lowland rain forest
in the Toraut region, pp. 197–254. In W. J. Knight and J. D. Holloway (eds.),
Insects and the rain forests of south east Asia (Wallacea). Royal Entomological
Society of London, London.
Hammond, P. M. 1992. Species inventory, pp. 17–39. In B. Groombridge (ed.), Global
biodiversity: status of the earth’s living resources. Chapman and Hall, London.
Harmon, M.E., J.F. Franklin, F.J. Swanson, P. Sollins, S.V. Gregory, J.D. Lattin,
N.H. Anderson, S.P. Cline, N.G. Aumen, and J.R. Sedell. 1986. Ecology of
coarse woody debris in temperate ecosystems. Adv. Ecol. Res. 15: 302.
Iidzuka, H., H. Goto, M. Yamasaki, and N. Osawa. 2014. Ambrosia beetles
(Curculionidae: Scolytinae and Platypodinae) on Fagus crenata Blume:
community structure, seasonal population trends and resource utilization patterns.
Entomol. Sci. 17: 167-180.
Jenkins, M.J., E. Hebertson, W. Page, and C.A. Jorgensen. 2008. Bark beetles, fuels,
fires and implications for forest management in the Intermountain West. For.
Ecol. Manage. 254: 16–34.
61
Johnson, D.W., and P.S. Curtis. 2001. Effects of forest management on soil C and N
storage: meta analysis. For. Ecol. Manage. 140: 227–238.
Kappes, H., M. Jabin, J. Kulfan, P. Zach, and W. Topp. 2009. Spatial patterns of
litter-dwelling taxa in relation to the amounts of coarse woody debris in European
temperate deciduous forests. For. Ecol. Manage. 257: 1255–1260.
Kashian, D.M., and J.A. Witter. 2011. Assessing the potential for ash canopy tree
replacement via current regeneration following emerald ash borer-caused
mortality on southeastern Michigan landscapes. For. Ecol. Manage. 261: 480–
488.
Kennedy, H.E Jr. 1990. Fraxinus pennsylvanica Marsh. Green ash, pp. 348–354. In R.
M. Burns, and B.H. Honkala (eds.), Silvics of North America: Hardwoods, vol. 2.
United States Department of Agriculture Forest Service Agricultural Handbook
654. Washington, DC.
Kimmerer, T.W., and T.T. Kozlowski. 1982. Ethylene, ethane, acetaldehyde, and
ethanol production by plants under stress. Plant Physiol. 69: 840-847.
Kurz, W.A., C. Dymond, G. Stinson, G. Rampley, E. Neilson, A. Carroll, T. Ebata,
and L. Safranyik. 2008. Mountain pine beetle and forest carbon feedback to
climate change. Nature. 452: 987–990.
Levin-Nielsen, A., and L.K. Rieske. 2014. Evaluating short term simulations of a forest
stand invaded by emerald ash borer. iForest doi: 10.3832/ifor1163-007.
Lindelöw, Å., B. Risberg, and K. Sjödin. 1992. Attraction during flight of scolytids and
other bark-and wood-dwelling beetles to volatiles from fresh and stored spruce
wood. Can. J. For. Res. 22: 224–228.
62
Lindgren, B.S. 1990. Ambrosia beetles. J. For. 88: 8-11.
Longcore, T. 2003. Terrestrial arthropods as indicators of ecological restoration success
in coastal sage scrub (California, USA). Restor. Ecol. 11: 397–409.
MacLean, D.A. 2004. Predicting forest insect disturbance regimes for use in emulating
natural disturbance, pp. 69–82. In A.H. Perera, L.J. Buse, M.G. Weber (ed.),
Emulating Natural Forest Landscape Disturbances: Concepts and Applications.
Columbia Univ. Press, NY.
Magurran, A.E. 2004. Measuring biological diversity. Blackwell Science, Oxford, UK.
Marshall, S.A. 2006. Insects: their natural history and diversity: with a photographic
guide to insects of eastern North America. Firefly Books, Buffalo, NY. 736 pp.
Mercado, J.E. 2010. Bark Beetle Genera of the United States. Colorado State University,
USDA-APHIS-PPQ Center for Plant Health Science and Technology, and USDA-
FS Rocky Mountain Research Station.
Montgomery, M.E., and P.M. Wargo. 1983. Ethanol and other host-derived volatiles as
attractants to beetles that bore into hardwoods. J. Chem. Ecol. 9: 181–190.
Novotny, V., S.E. Miller, L. Baje, S. Balagawi, Y. Basset, L. Cizek, K.J. Craft, F.
Dem, R.A. Drew, and J. Hulcr. 2010. Guild‐specific patterns of species richness
and host specialization in plant–herbivore food webs from a tropical forest. J.
Anim. Ecol. 79: 1193-1203.
Perkins, T.D., H.W. Vogelmann, and R.M. Klein. 1987. Changes in light intensity and
soil temperature as a result of forest decline on Camels Hump, Vermont. Can. J.
For. Res. 17: 565–568.
63
Pimentel, D., R. Zuniga, and D. Morrison. 2005. Update on the environmental and
economic costs associated with alien-invasive species in the United States. Ecol.
Econ. 52: 273–288.
Poland, T.M., and D.G. McCullough. 2006. Emerald ash borer: invasion of the urban
forest and the threat to North America’s ash resource. J. For. 104: 118–124.
Rabaglia, R.J., S.A. Dole, and A.I. Cognato. 2006. Review of American Xyleborina
(Coleoptera: Curculionidae: Scolytinae) occurring north of Mexico, with an
illustrated key. Ann. Entomol. Soc. Am. 99: 1034-1056.
Root, R.B. 1967. The niche exploitation pattern of the blue-gray gnatcatcher. Ecol.
Monogr. 37: 317-350.
SAS Institute. 2011. SAS/IML 9.3 user’s guide. SAS Institute, Cary, NC.
Schlesinger, R. C. 1990. Fraxinus americana L. white ash, pp. 654–665. In R. H.
Russell, and B. H. Honkala (eds.), Silvics of North America: Hardwoods, vol. 2.
United States Department of Agriculture Forest Service Agricultural Handbook
654. Washington, DC.
Schowalter, T.D. 2012. Insect responses to major landscape-level disturbance. Annu.
Rev. Entomol. 57: 1–20.
Schowalter, T.D., D.C. Lightfoot, and W.G. Whitford. 1999. Diversity of arthropod
responses to host-plant water stress in a desert ecosystem in southern New
Mexico. Am. Midl. Nat. 142: 281–290.
Schowalter, T.D, and M.D. Lowman. 1999. Forest herbivory by insects, pp. 269–285.
In L.R. Walker (ed.), Ecosystems of the World: Ecosystems of Disturbed Ground.
Amsterdam: Elsevier.
64
Schowalter, T.D. 1985. Adaptations of insects to disturbance, pp. 235–252. In S.T.
Pickett, P.S. White (ed.), The Ecology of Natural Disturbance abd Patch
Dynamics. Orlando, FL.
Schowalter, T.D., and L.M. Ganio. 2003. Diel, seasonal and disturbance-induced
variation in invertebrate assemblages, pp. 315–328. In Y. Basset, V. Novotny,
S.E. Miller, R.L. Kitching (ed.), Arthropods of Tropical Forests. Cambridge
University Press, Cambridge, UK.
Shure, D.J., and L.A. Wilson. 1993. Patch-size effects on plant phenolics in
successional openings of the southern Appalachians. Ecology. 74: 55–67.
Simberloff, D., and B. Von Holle. 1999. Positive interactions of nonindigenous species:
invasional meltdown? Biol. Invasions. 1: 21-32.
Swift, M., I. Healey, J. Hibberd, J. Sykes, V. Bampoe, and M. Nesbitt. 1976. The
decomposition of branch-wood in the canopy and floor of a mixed deciduous
woodland. Oecologia. 26: 139–149.
Tanis, S.R., and D.G. McCullough. 2012. Differential persistence of blue ash and white
ash following emerald ash borer invasion. Can. J. For. Res. 42:1542–1550.
Triplehorn, C.A., and N.F. Johnson. 2005. Borror and DeLong's Introduction to the
Study of Insects. Brooks/Cole, Belmont, CA. 888 pp.
Ulyshen, M.D. 2014. Wood decomposition as influenced by invertebrates. Biological
Reviews. 91: 70–85.
USDA APHIS. 2016. U.S. Department of Agriculture Animal and Plant Health
Inspection Service cooperative emerald ash borer project: Initial county EAB
65
detections in North America. (http://www.
emeraldashborer.info/files/MultiState_EABpos.pdf) (Accessed 01 Feb. 2016).
USDA Forest Service. 2009. Common stand exam user’s guide, Chap. 2.
(http://www.fs.fed.us/nrm/fsveg/) (Accessed 01 Feb. 2016).
Van Bael, S.A., A. Aiello, A. Valderrama, E. Medianero, M. Samaniego, and S.J.
Wright. 2004. General herbivore outbreak following an El Nino-related drought
in a lowland Panamanian forest. J. Trop. Ecol. 20: 625–633.
Vanderwel, M.C., J.R. Malcolm, and S.M. Smith. 2006a. An integrated model for snag
and downed woody debris decay class transitions. For. Ecol. Manage. 234: 48–59.
Vanderwel, M. C., J. R. Malcolm, S. M. Smith, and N. Islam. 2006b. Insect
community composition and trophic guild structure in decaying logs from eastern
canadian pine dominated forests. For. Ecol. Manage. 225:190–199.
Walker, L.R., and M.R. Willig. 1999. An introduction to terrestrial disturbance, pp. 1-
16. In L.R. Walker (ed.), Ecosystems if the World: Ecosystems of Disturbed
Ground. Amsterdam: Elsevier.
Wharton, M.E., and R.W. Barbour. 1973. Trees and Shrubs of Kentucky, University
Press of Kentucky. Lexington, KY. 582 pp.
White, P.S., and S. Pickett. 1985. Natural disturbance and patch dynamics: an
introduction, pp. 3–13. In S.T. Pickett, P.S. White (ed.), The Ecology of Natural
Disturbance abd Patch Dynamics. Orlando, FL.
Wilcove, D.S., D. Rothstein, J. Dubow, A. Phillips, and E. Losos. 1998. Quantifying
threats to imperiled species in the United States: assessing the relative importance
66
of habitat destruction, alien species, pollution, overexploitation, and disease.
Bioscience. 48: 607–615.
Zhang, Q., and Y. Liang. 1995. Effects of gap size on nutrient release from plant litter
decomposition in a natural forest ecosystem. Can. J. For. Res. 25: 1627–1638.
67
VITA
Matthew Bryant Savage
Education:
• University of Kentucky, B.S. in Forestry, May 2014
Employment:
• Exotic Plant Management Team (Crew Leader) – Supervisor: Steven Bekedam, Yellowstone National Park, May 2017 – Present
• Field Research Technicain – Supervisor: Eric Chapman, Ministry of Agriculture and Fisheries in Muscat, Oman, February – March 2017
• Biological Science Technician (Plants) – Supervisor: Brian Hoefling, Uncompahgre National Forest, May – October 2016
• Undergraduate Field/Lab Technician – Supervisor: Dr. Lynne Rieske-Kinney, Department of Entomology, University of Kentucky, August 2013 – May 2014
• Forestry Technician – Supervisor: Ron Hollis, White River National Wildlife Refuge, May – August 2012 and May – August 2013
Awards:
• Graduate Student Grant – Kentucky Native Plant Society, October 2015 • Graduate Student Oral Presentation (2nd Place) – Southern Forest Insect Work
Conference, July 2015
Oral Presentaations:
• University of Kentucky, Department of Entomology, MS Exit Seminar, March 2016
• Southern Appalachian Forest Entomology and Pathology Symposium, March 2016
• 5th Annual Sustainability Forum Poster Competition: Tracy Farmer Institute for Sustainability of the Environment, December 2015
• Southern Forest Insect Work Conference Graduate Student Competition, July 2015
• University of Kentucky, Department of Entomology, MS Proposal Seminar, January 2015
• Ohio Valley Entomological Association Graduate Student Competition, October 2014