Technology Transfer Non-native Pest

Edited by Roy G. Van Driesche and Richard C. Reardon

Forest Health Technology Enterprise 

Team Morgantown, WV

United States Department of Agriculture

Forest Service FHTET-2014-09 March 2015

Biology and Control

of Emerald Ash Borer
On the cover: Cover design by Sheryl Romero and Denise Binion, Forest Health Technology 

Enterprise Team. Background image: Understory green ash seedlings (Fraxinus pennsylvanica, 

Oleaceae) released after large ash trees were killed by emerald ash borer in Okemos, Michigan 

in 2014, photo by Leah S. Bauer; (bottom row, left to right) Fully mature Tetrastrichus planipennisi 

larvae break free of emerald ash borer larval skin and pupate in the larval gallery under the tree 

bark. (Photo credit: Clifford Sadof); EAB adult and typical leaf feeding damage. (Photo credit: 

Deborah Miller, USDA Forest Service, Bugwood.org); Emerging Tetrastrichus plannipennisi adults. 

(Photo credit Leah S. Bauer).

The Forest Health Technology Enterprise Team (FHTE T ) was created in 1995 

by the Deputy Chief for State and Private Forestry, USDA Forest Service, to develop and deliver 

technologies to protect and improve the health of American forests. This book was published 

by FHTET as part of the technology transfer series.

http://www.fs.fed.us/foresthealth/technology/

The U.S. Department of Agriculture (USDA) prohibits discrimination in all its programs and 

activities on the basis of race, color, national origin, sex, religion, age, disability, political 

beliefs, sexual orientation, or marital or family status. (Not all prohibited bases apply to all 

programs.) Persons with disabilities who require alternative means for communication of 

program information (Braille, large print, audiotape, etc.) should contact USDA’s TARGET 

Center at 202-720-2600 (voice and TDD).

To file a complaint of discrimination, write USDA, Director, Office of Civil Rights, Room 326-

W, Whitten Building, 1400 Independence Avenue, SW, Washington, D.C. 20250-9410, or 

call 202-720-5964 (voice and TDD). USDA is an equal opportunity provider and employer.

Richard Reardon 

USDA Forest Service

180 Canfield St. 

Morgantown, WV 26505 

(304) 285-1566

rreardon@fs.fed.us

For additional copies of this publication, contact:

Roy Van Dreische 

Department of Environmental Conservation 

Holdsworth Hall 

University of Massachusetts, Amherst, MA 01003

(413) 545-1061

vandries@cns.umass.edu

The entire publication is available online at:

http://www.fs.fed.us/foresthealth/technology/pdfs/FHTET-2014-09_Biology_Control_EAB.pdf

We thank the authors of the individual chapters for their expertise in reviewing and summarizing the 

literature and providing current information on the biology and control of emerald ash borer. Thanks to 

Denise Binion for layout and design of this publication. We would also like to thank the U. S. Department 

of Agriculture, Forest Service, Agricultural Research Service and Animal and Plant Health Inspection 

Service for technical and financial support and Forest Health Technology Enterprise Team for providing 

funding for the preparation and printing of this publication.
Biology and Control

of Emerald Ash Borer

FHTET-2014-09

March 2015

Edited by 

Roy G. Van Driesche

Richard C. Reardon

Table of Contents

Chapter 1: Emerald Ash Borer Biology and Invasion History

By Robert A. Haack, Yuri Baranchikov, Leah S. Bauer, and Therese M. Poland ................................1

Chapter 2: Ecological Impacts of Emerald Ash Borer

By David L. Wagner and Katherine J. Todd ..................................................................................... 15

Chapter 3: Host Range and Host Resistance

By Daniel A. Herms ......................................................................................................................... 65

Chapter 4: Other Options for Emerald Ash Borer Management: Eradication and

Chemical Control

By Deborah G. McCullough .......................................................................................................... 75

Chapter 5: History of Emerald Ash Borer Biological Control

By Juli R. Gould, Leah S. Bauer, Jian J. Duan, David Williams, and Houping Liu .......................... 83

Chapter 6: Biology of Emerald Ash Borer Parasitioids

By Leah S. Bauer, Jian J. Duan, Jonathan P. Lelito, Houping Liu, and Juli R. Gould....................... 97

Chapter 7: Trapping Techniques for Emerald Ash borer and Its Introduced

Parasitoids

By Kristopher Abell, Therese Poland, Allard Cossé and Leah Bauer............................................113

Chapter 8: Mass-rearing of Emerald Ash Borer and its Parasitoids

By Jonathan P. Lelito, Timothy J. Watt, and Jian J. Duan .............................................................129

Chapter 9: Life Table Evaluation of Change in Emerald Ash Borer Populations

Due to Biological Control

By David E. Jennings, Jian J. Duan, Kristopher J. Abell, Leah S. Bauer, Juli R. Gould, 

Paula M. Shrewsbury and Roy G. Van Driesche ...........................................................................139

Chapter 10: Risk to Ash from Emerald Ash Borer: Can Biological Control

Prevent the Loss of Ash Stands?

By Jian J. Duan, Roy G. Van Driesche, Leah S. Bauer, Daniel M. Kashian, and Daniel A. Herms ..153

Chapter 11: Future Directions in EAB-Affected Forests

By Deborah G. McCullough, Roy Van Driesche and Therese M. Poland .....................................165

1 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Chapter 1: emerald ash Borer Biology and invasion history 

Robert A. Haack,1 Yuri Baranchikov,2 Leah S. Bauer,1 and Therese M. Poland1 

1

USDA Forest Service, Northern Research Station, 3101 Technology Blvd., Suite F, Lansing, Michigan 48910
 

2

V.N.Sukachev Institute of Forest, Siberian Branch, Russian Academy of Science, 


50 Akademgorodok, 660036 Krasnoyarsk, Russian Federation
 

introdUCtion 

The emerald ash borer (EAB), Agrilus planipennis 

Fairmaire (Coleoptera: Buprestidae), is native 

to eastern Asia and is primarily a pest of ash 

(Fraxinus) trees (Fig. 1). Established populations 

of EAB were first detected in the United States and 

Canada in 2002 (Haack et al., 2002), and based on 

a dendrochronology study by Siegert et al. (2009), 

the original EAB introduction likely occurred in 

the early to mid-1990s in Michigan. In European 

Russia, EAB was first found near Moscow in 2003, 

but not officially identified until 2005 (Izhevskii 

and Mozolevskaya, 2010). EAB has become a 

serious pest of ash in North America and European 

Russia, is causing widespread tree mortality, and is 

spreading rapidly on both continents (Cappaert et 

al., 2005; Poland and McCullough, 2006; Kovacs et 

al., 2010; Baranchikov, 2013; EAB Info, 2013; OrlovaBienkowskaja, 2013; Straw et al., 2013; Herms and 

McCullough, 2014). In this chapter, we discuss the 

biology of EAB, its native and introduced range 

through 2013, and the likely pathways by which it was 

introduced and spread. 

General Biology 

The life cycle of EAB is typically completed in one 

year, but two years is often required, especially in 

vigorous hosts, in cooler climates, or when eggs are 

laid late in the season (Cappaert et al., 2005; Wei 

et al., 2007; Wang et al., 2010). In addition, Petrice 

and Haack (2007) reported that EAB may require 

two years to complete development in cut logs or 

firewood, especially when the wood has dried. EAB 

can successfully infest both healthy and stressed ash 

Figure 1. Adult emerald ash borer (EAB), Agrilus planipennis 

Fairmaire (Coleoptera: Buprestidae). (Photo credit: David 

Cappaert, Michigan State University, Bugwood.org) 

trees in North America and European Russia, 

where the native ash species did not coevolve with 

EAB (Liu et al., 2003; Wei et al., 2004; Poland and 

McCullough, 2006; Baranchikov et al., 2008; Rebek 

et al., 2008). However, within EAB’s native range 

in China and the Russian Far East, species of Asian 

ash are usually resistant to the borer, except during 

periods of environmental stress such as prolonged 

drought (Yu, 1992; Zhao et al., 2005; Baranchikov 

et al., 2008). In addition, EAB has been reported to 

kill species of North American ash that were planted 

in China and Russia (Liu et al., 2003; Zhao et al., 

2005; Baranchikov et al., 2008). EAB infests nearly 

all sizes of ash trees, from saplings that measure 2-3 

cm in diameter to mature trees (Haack et al., 2002; 

Wei et al., 2007), and infests both open-grown and 

interior-forest trees (Poland and McCullough, 2006; 

McCullough et al., 2009; Wang et al., 2010) (Figs. 

2-3). 

In China and the Russian Far East, the principal 

native hosts of EAB include Fraxinus mandshurica 

Ruprecht and Fraxinus chinensis Roxburgh (Yu, 1992; 

Zhao et al., 2005; Wei et al., 2007; Baranchikov et al., 
2 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

2008; Izhevskii and Mozolevskaya, 2010), whereas 

in North America, EAB has been able to infest and 

kill all species of native Fraxinus so far encountered, 

including F. americana L., F. nigra Marshall, F. 

pennsylvanica Marshall, F. profunda (Bush) Bush, 

and F. quadrangulata Michx. (Anulewicz et al., 2008; 

EPPO, 2013). In European Russia, EAB has infested 

and killed primarily the introduced North American 

species F. pennsylvanica and the native European 

species Fraxinus excelsior L. (Baranchikov et al., 2008; 

Izhevskii and Mozolevskaya, 2010; Duan et al., 2012). 

It is important to note that Jendek (1994) 

synonymized two other Asian Agrilus species and one 

subspecies with A. planipennis, type China (EAB), 

including Agrilus feretrius Obenberger (type Taiwan), 

Agrilus marcopoli Obenberger (type Mongolia), 

and Agrilus marcopoli ulmi Kurosawa (type Japan) 

(Jendek and Grebennikov, 2011). Besides ash, which 

is the only larval host reported for A. planipennis in 

China (Yu, 1992; Liu et al., 2003; Zhao et al., 2005), 

other tree genera (Juglans, Pterocarya, and Ulmus) 

were reported as larval hosts in Korea and Japan 

for A. marcopoli and A. marcopoli ulmi (Ko, 1969; 

Akiyama and Ohmomo, 1997). However, in a recent 

EAB pest risk assessment prepared by the European 

and Mediterranean Plant Protection Organization 

(EPPO, 2013), it was reported that Japanese buprestid 

specialists now consider the non-Fraxinus host 

records for Japan to be in error. 

The adult flight season of EAB usually begins 

in May or June in the Great Lakes region of North 

America and at similar latitudes in Asia, with peak 

flight occurring in June to July, and usually ending 

by September (Cappaert et al., 2005; Wei et al., 2007; 

Wang et al., 2010). Adults are most active on sunny 

days when air temperatures exceed 25° C (Wang et 

al., 2010), but during rainy or cool weather the adults 

often rest in bark crevices and on leaves (RodriguezSaona et al., 2007). EAB adults consume host foliage 

throughout their life and can live for several weeks 

under favorable laboratory conditions (Fig. 4; Wang 

et al., 2010; EPPO, 2013). 

EAB adults use visual and olfactory cues to locate 

host trees and mates. Shades of purple and green 

are highly attractive to EAB adults (Francese et al., 

2005, 2008, 2010; Crook et al., 2009). Moreover, EAB 

Figure 2. Recently planted ash trees showing thinning crowns 

and epicormic shoots typical of EAB infestation. (Photo credit: 

Leah Bauer, USDA Forest Service, Bugwood.org) 

Figure 3. Mature ash tree showing dieback typical of EAB 

infestation and bark removal by woodpeckers as they search 

for EAB life stages. (Photo credit: Steven Katovich, USDA Forest 

Service, Bugwood.org) 
CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

3 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

 

adults are attracted to dead EAB adults when placed 

on foliage or traps as decoys (Lelito et al., 2007, 2008; 

Petrice et al., 2013). This is not surprising given that 

EAB adult males are known to hover near host trees 

when searching for mates, and then landing on or near 

prospective mates when they are located (Lelito et al., 

2007; Rodriguez-Saona et al., 2007). Various volatiles 

from ash bark and foliage elicit positive responses in 

EAB adults under laboratory conditions, and some of 

these compounds increase EAB attraction to purple 

or green traps (Rodriguez-Saona et al., 2006; Crook et 

al., 2008; Crook and Mastro, 2010; Grant et al., 2011; 

Poland et al., 2011; Poland and McCullough, 2014). 

Also, close range sex pheromones have been identified 

for EAB, and field testing has found them to increase 

attraction of EAB to traps (Lelito et al., 2009; Silk et al., 

2011; Ryall et al., 2012). 

EAB adults mate on the trunk, branches, and 

foliage of their host plants. Oviposition usually begins 

about 5-10 days after adult emergence. Eggs are laid 

individually or in small clusters between layers of bark 

and in bark crevices along the trunk, major branches, 

and exposed roots (Wei et al., 2007; Anulewicz et al., 

2008; Wang et al., 2010; Jennings et al., 2014) (Fig. 

5). Under laboratory conditions, average adult female 

longevity is about 7-9 weeks, with total fecundity 

usually averaging between 40 to 74 eggs per female and 

with a maximum of 307 eggs (Rutledge and Keena, 

2012; Jennings et al., 2014). Average EAB adult male 

longevity is about 43 days (EPPO, 2013). 

Egg hatch usually occurs after 7-18 days, 

depending on local temperatures. Neonate larvae chew 

through the surface of the egg that is in contact with 

the tree, and tunnel directly through the outer bark 

to the cambial region where they feed on the inner 

bark (phloem) and outer sapwood, creating frassfilled galleries (Wei et al., 2007; Wang et al., 2010). 

Larval galleries tend to be more serpentine-shaped in 

vigorous host trees (Fig. 6), while more meandering in 

less vigorous hosts or when larval densities are high 

(Wei et al., 2007; Wang et al., 2010) (Fig. 7). 

Chamorro et al. (2012) described the morphology 

of EAB eggs, larvae, and pupae in great detail. Briefly, 

EAB has four larval instars, and as is typical of larvae 

in the genus Agrilus, there are two heavily sclerotized 

processes, often called urogomphi, at the terminal 

Figure 4. Typical leaf feeding damage by EAB adults. (Photo 

credit: Deborah Miller, USDA Forest Service, Bugwood.org) 

a

b

Figure 5. EAB eggs are white in color when first deposited (a) 

and then turn yellowish-brown within a few days (b). (Photo 

credit: Houping Liu, Michigan State University, Bugwood.org) 
4 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

end of the abdomen (Fig. 8). Measurements of the 

urogomphi can be used to distinguish the larval 

instars (Liu et al., 2007; Petrice et al., 2009; Wang et 

al., 2010). For individuals that complete their life 

cycle in one year, larvae overwinter as mature fourth 

instars (Cappaert et al., 2005; Wang et al., 2005, 2010). 

For individuals that develop over two years, the first 

winter is usually spent as early instar larvae. Once a 

larva completes its feeding as a fourth instar (Fig. 9) it 

constructs a pupal cell, usually in the outer sapwood 

of thin-barked branches or trees or in the outer bark 

of thick-barked trees (Abell et al., 2012). Before 

creating the pupal cell, 4th-instar larvae construct a 

tunnel that extends nearly to the surface of the outer 

bark that will later be used by the new adult when 

it exits the tree (Wang et al., 2010). In the newly 

completed pupal cell, the 4th-instar larva folds itself 

into a J-shape or U-shape before overwintering (Fig. 

10). 

In spring, the larvae that overwintered in pupal 

cells develop into prepupae by gradually unfolding 

their body as they become shorter and more 

cylindrical. Prepupae then molt into naked or exarate 

pupae (Wang et al., 2010). Pupation occurs in late 

spring and early summer and usually lasts 3-4 weeks 

(Fig. 11). After eclosion, the newly formed or pharate 

adult will remain in its pupal cell for about one week 

before it chews its way out of the tree by enlarging 

the exit tunnel that it created earlier when it was a 

mature larva (Wei et al., 2007; Wang et al., 2010). 

The exit hole constructed by the adults is typically 

D-shaped, with the flat side of the “D” corresponding 

Figure 6. EAB larval gallery in a vigorous host as evidenced by 

the tight zig-zag pattern of the gallery and the attempt by the 

tree to compartmentalize the gallery. (Photo credit: Edward 

Czerwinski, Ontario Ministry of Natural Resources, Bugwood) 

Figure 8. Close-up of the paired terminal processes found at 

the tip of the last abdominal segment of EAB larvae. (Photo 

credit: Pennsylvania Department of Conservation and Natural 

Resources, Bugwood.org) 

Figure 7. EAB larval galleries on a less-vigorous host tree 

as evidenced by the meandering pattern of the galleries. 

(Photo credit: Edward Czerwinski, Ontario Ministry of Natural 

Resources, Bugwood.org) 

Figure 9. Fourth instar EAB in its gallery, which is constructed 

in the cambial region of the tree. (Photo credit: Pennsylvania 

Department of Conservation and Natural Resources, 

Bugwood.org) 
CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

5 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

to the upper side of the adult’s body (Fig. 12). Upon 

emergence, adults readily walk or fly to host foliage 

and feed (Wang et al., 2010). 

As is typical for many Agrilus species, trees often 

die after 1-3 years of successive borer infestation, with 

death usually beginning in the crown branches and 

moving downward in subsequent years to the main 

trunk (Haack and Benjamin, 1982; Cappaert et al., 

2005; Ryall et al., 2011; Foelker et al., 2013). However, 

in small diameter ash trees, initial EAB infestations 

often begin on the main trunk (Timms et al., 2006; 

Wei et al., 2007; Tluczek et al., 2011). In many EABinfested ash trees, epicormic branches develop along 

the lower trunk before the tree dies (Cappaert et al., 

2005; Wang et al., 2010) (Figs. 2, 13). 

Native Range of Emerald Ash Borer 

EAB is native to China, Japan, Korea, Mongolia, the 

Russian Far-East, and Taiwan (Yu, 1992; Jendek, 1994; 

Jendek and Grebennikov, 2011; Chamorro et al., 

2014). The recent report of EAB from Laos (Jendek 

and Grebennikov, 2011) is no longer considered valid 

given that the specimens examined from Laos were 

later described as a new species: Agrilus tomentipennis 

(Jendek and Chamorro, 2012). Although EPPO 

(2013) raised doubts on the occurrence of EAB in 

Mongolia, Jendek and Grebennikov (2011) state that 

the type specimen for A. marcopoli is from Mongolia. 

In addition, as stated above, the occurrence of EAB 

in Japan and Taiwan is based on specimens that 

were formerly considered A. marcopoli ulmi and 

A. feretrius, respectively (Jendek, 1994; Jendek and 

Grebennikov, 2011). 

initial disCovery and spread oF 

eaB in north ameriCa 

EAB was first discovered in North America in 2002 

(Haack et al., 2002; Cappaert et al., 2005; Poland and 

McCullough, 2006; Herms and McCullough, 2014). 

The first adults were reared from declining ash trees 

near Detroit, Michigan, in May 2002, and were sent to 

several taxonomists for identification. Later, in July 

2002, they were positively identified as A. planipennis 

by Eduard Jendek in Slovakia, who is the world 

Figure 10. Fourth instar EAB larvae in their typical 

overwintering position (J-larvae) inside pupal cells that were 

constructed in the outer sapwood. (Photo credit: Houping Liu, 

Michigan State University, Bugwood.org) 

Figure 11. EAB pupae are naked and gradually mature into 

adults within their individual pupal cells during spring and 

summer. (Photo credit: Deborah Miller, USDA Forest Service) 

authority on Asian Agrilus. Moreover, beetles that 

looked similar to EAB were collected in July 2002 in 

Windsor, Ontario, and identified as EAB in August 

2002. 

Michigan and Canada enacted quarantines on 

all known EAB-infested counties starting in July 

and September 2002, respectively (Haack et al., 

2002). A federal EAB quarantine was first enacted 
6 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

 

in the United States in October 2003 (USDA APHIS, 

2003). The EAB quarantine zone has expanded 

each year since 2002 in both the United States and 

Canada as a result of regional surveys in several states 

and provinces. When new EAB populations were 

discovered, quarantines were usually enacted at the 

county level. As a result of intense survey efforts, 

the steady range expansion of EAB has been well 

documented in North America (Fig. 14). However, 

it is important to realize that it usually takes several 

years before EAB populations are large enough to 

be detected during surveys. Range expansion of 

EAB is a result of both natural spread and artificial 

movement of infested ash material. 

By the end of 2002, EAB had been found in six 

southeastern Michigan counties in the Detroit area. 

This number increased to 13 counties by the end of 

2003, and 20 by 2004, all still within Michigan’s Lower 

Peninsula. In 2005, EAB was found for the first 

time in Michigan’s Upper Peninsula. EAB was first 

found in Ohio in 2003; Indiana in 2004; Illinois and 

Maryland in 2006; Pennsylvania and West Virginia 

in 2007; Wisconsin, Missouri and Virginia in 2008; 

Minnesota, New York, and Kentucky in 2009; Iowa 

and Tennessee in 2010; Connecticut, Kansas, and 

Massachusetts in 2012; and Colorado, Georgia, New 

Hampshire, and North Carolina in 2013 (EAB Info, 

2013) (Fig. 14). In Canada, EAB has been detected in 

just two provinces as of 2013, first in Ontario in 2002, 

and then in Quebec in 2008 (Fig. 14). Overall, as of 

December 2013, EAB was known to occur in 22 U.S. 

states and two Canadian provinces. 

introdUCed range and spread 

oF eaB in rUssia 

There are few early records of EAB from Russia. 

During the 1900s, all EAB records were from 

southern Primorskiy Kray in the Russian Far East and 

consisted of small numbers of specimens collected 

during 1935-1999 (Alekseyev, 1979; Jendek, 1994; 

Volkovich, 2007; Yurchenko et al., 2007; Fig. 15). In 

2004, EAB populations were also found in southern 

Khabarovsk Kray in the Russian Far East in the 

area between Khabarovsk and Dzonki, a distance of 

about 100 km as measured along the Amur River 

Figure 12. EAB adults construct D-shaped exit holes as they 

chew through the bark and emerge from their host tree. 

(Photo credit: Deborah Miller, USDA Forest Service) 

Figure 13. EAB infested ash tree with epicormic shoots that 

often develop during the latter years of infestation prior to 

tree death. (Photo credit: Edward Czerwinski, Ontario Ministry 

of Natural Resources, Bugwood.org) 
CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

7 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Figure 14. (top) Annual spread of EAB in North America from 2002 through 2013 as determined by year of first detection. 

Service layer credits: US National Park Service. Data sources: USDA Animal & Plant Health Inspection Service (APHIS), Canadian 

Food Inspection Agency (CFIA). Map developed by USDA Forest Service, Northeastern Area State and Private Forestry, Office of 

Knowledge Management (T. Luther 04/15/2014). 

Figure 15. (bottom) Known range of EAB in Asia and introduced area of EAB in European Russia as of 2013. Service layer credits: 

US National Park Service. Data sources: https://sites.google.com/site/eduardjendek/world-distribution-of-agrilus-plannipennis_ 

and Baranchikov (2013). Map developed by USDA Forest Service, Northeastern Area State and Private Foresty, Office of 

Knowledge Management (T. Luther 04/15/2014). 
8 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

 

(Yurchenko, 2010; Fig. 15). 

Historically, EAB was a rare species in the 

Russian Far East, where it was associated exclusively 

with weakened and dying local native ash trees such 

as F. mandshurica and F. chinensis. Widespread tree 

mortality associated with EAB was first noticed in 

the Russian Far East in 2004, affecting introduced 

North American ash trees (F. pennsylvanica) that were 

growing along streets in Vladivostok (Yurchenko, 

2010), many of which were rather mature trees with 

trunks measuring 20-40 cm in diameter. Subsequent 

detailed investigations of dead North American ash 

trees (F. americana and F. pennsylvanica ) in parks 

and arboreta in Khabarovsk demonstrated that these 

trees had been killed by EAB during the previous 

5-10 years when the trees were 28-35 years old 

(Yurchenko, 2010). 

In European Russia, beetles that were later to 

be identified as EAB were first collected on the 

streets of Moscow in June 2003 (Fig. 15; Volkovich, 

2007). These beetles were positively identified as 

A. planipennis in 2005 by A. B. Alekseyev – the 

leading Russian expert on Buprestidae (Izhevskii and 

Mozolevskaya, 2010). It was soon recognized that 

EAB was responsible for the widespread ash dieback 

in Moscow (Baranchikov et al., 2008; Mozolevskaya 

et al., 2008). From 2006-2013, EAB spread outward 

from Moscow (Fig. 15). In 2006, 10 EAB adults 

were collected 30 km west of the Moscow Ring 

Highway (Volkovich, 2007), and by 2009, EABkilled ash trees were found in many settlements of 

the Moscow Oblast region, with the most westward 

known infestation in Mozhaisk, about 100 km from 

Moscow (Baranchikov et al., 2010a). EAB was found 

in the Kaluga Region in 2010, and in the Smolensk 

and Ryazan Regions in 2012 (Baranchikov and 

Kurteyev, 2012; Baranchikov, 2013). Similarly, in 

2013, EAB was first reported in the Orel, Tambov, 

Tula, Tver, Vladimir, Voronezh, and Yaroslavl Regions 

(Baranchikov, 2013, Orlova-Bienkovskaya, 2013). 

The current known range of EAB in European Russia 

is close to the borders of Belarus and Ukraine (Fig. 15). 

Special EAB surveys were conducted during 

2008-2009 on F. pennsylvanica in several cities 

throughout southern Siberia (Abakan, Krasnoyarsk, 

Novosibirsk, Tomsk, and Ulan-Ude) and the central 

Urals (Yekaterinburg). However, no additional 

EAB populations were found during these surveys 

(Baranchikov et al., 2010b). 

pathWays oF emerald ash Borer 

dispersal 

It is not known for certain how EAB reached North 

America or European Russia. In North America, 

wood packaging material such as pallets and crating 

from Asia is considered the most likely source 

(Haack et al., 2002, Cappaert et al., 2005, Haack, 

2006). Recent genetic analyses by Bray et al. (2011) 

and Keever et al. (2013) found that North American 

EAB populations were most similar to Chinese 

populations, less so with Korean populations, 

and least similar to Japanese populations. As for 

European Russia, Izhevskii and Mozolevskaya (2010) 

suggested that EAB could have been introduced on 

ash nursery stock imported from North America 

or on wood packaging material from Asia. Genetic 

analyses may not help determine the source of the 

Moscow EAB population because molecular testing 

has shown high similarity among North American, 

Chinese, Far-East Russian, and Moscow EAB 

populations (EPPO 2013). 

In North America and Europe, EAB can spread 

naturally through adult flight, which can expand 

the infested area by several kilometers each year 

(Taylor et al., 2010; EPPO, 2013). However, EAB 

dispersal over distances of 10s or 100s of kilometers 

most likely results from human movement of 

infested host material such as ash nursery stock, 

logs, and firewood (Cappaert et al., 2005; Haack, 

2006; Poland and McCullough, 2006; Haack et al., 

2010; Herms and McCullough, 2014). For example, 

a nursery in Michigan sold EAB-infested nursery 

stock to a Maryland nursery in 2003, which then 

sold some of the trees to individuals living in 

Maryland and Virginia before realizing the trees 

were infested (Muirhead et al., 2006). Similarly, a 

sawmill near Shipshewana, Indiana, which regularly 

purchased ash sawlogs from southern Michigan was 

apparently responsible for introducing EAB to the 

local area (Robertson and Andow, 2009). Firewood 

is believed to be a major pathway by which EAB 
CHAPTER 1: EMERALD ASH BORER BIOLOGY AND INVASION HISTORY

9 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

has been introduced to many residential areas, 

vacation properties, and campgrounds (McCullough 

et al., 2003; Robertson and Andow, 2009; Haack 

et al., 2010). In addition, EAB adults have been 

documented to hitchhike on or inside vehicles, as 

well as on passengers, which may explain their high 

frequency of establishment along major highways, 

especially at rest areas and truck stops (Buck and 

Marshall, 2008). The means of long-distance EAB 

dispersal in European Russia is not clear given that 

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Chapter 2: eCologiCal impaCts oF emerald ash Borer 

David L. Wagner1 and Katherine J. Todd2 

1

Corresponding author, Center for Conservation and Biodiversity, Department of Ecology and Evolutionary Biology, 

University Box 43, University of Connecticut, Connecticut 06269, david.wagner@uconn.edu (860)486-2139 

2

Department of Entomology, The Ohio State University, Columbus, Ohio 43210, todd.489@osu.edu 

introdUCtion 

The genus Fraxinus includes 16 North American 

species. Flowers et al. (2013) estimate that there are 

more than 8.7 billion ash trees and saplings in the 

continental United States, and these are all potentially 

susceptible to emerald ash borer (EAB) (Agrilus 

planipennis Fairmaire) infestation. Since its invasion, 

this beetle has established in more than 20 states, 

from Minnesota to Maine, south to Georgia and 

Missouri, as well as in southern Ontario and Quebec, 

and is expanding its range on all edges of its current 

distribution. Because timber and firewood from 

infested areas can be transported long distances, the 

beetle has the potential to establish virtually anywhere 

where ash species grow. It is considered to be among 

the most destructive forest insect pests to have 

been introduced into North America (Herms and 

McCullough, 2014; McCullough and Usborne, 2014). 

More than 200,000 million ash trees have been killed 

– especially in the Great Lakes region where the 

insect first established in the early 1990s (Cappaert et 

al., 2005a; Poland and McCullough, 2006, Siegert et 

1 2 

3 4 

Figures 1-4. Affected communities in Ohio; dead trees are green ash (F. pennsylvanica) killed by the emerald ash borer: (1) Saint 

Mary’s River west of Decatur, June 2014. (Photo courtesy Jim McCormac); (2) Willow Point Wildlife Area in Vickery, August 2011. 

(Photo courtesy Jim McCormac); (3, 4) Ottawa National Wildlife Refuge in Oak Harbor, August 2014. (Photos courtesy Judy 

Semroc) 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

16 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

al., 2007) (Figs. 1-4). 

Fraxinus americana L. (white ash) and especially 

Fraxinus pennsylvanica Marshall (green ash) – strong, 

stately, rapidly growing trees – are widely planted in 

yards, parks, and along city streets, in part because 

both species are known to be hardy and relatively 

insect- and disease-free (Burns and Honkala, 1990). 

Ash is also preferred for firewood because its sap 

is flammable and, as such, the potential for EAB to 

be spread throughout North America by human 

transport of infested wood is greatly heightened. 

A lower bound economic estimate for treating, 

removing, and replacing EAB-infested ash trees in 

urban landscapes for 2010 to 2020 is $12.5 billion 

(Kovacs et al., 2011). White ash and, to a lesser extent, 

green ash are commercially important trees whose 

strong but flexible wood is used for flooring, paneling, 

furniture, tool handles, and baseball bats (Elias, 1987; 

Burns and Honkala, 1990). White ash has long been 

the preferred wood for the Louisville Slugger – a bat 

popular with professional baseball players. 

Ash typically grows as a component in hardwood 

forests (Figs. 5-11); furthermore, Fraxinus species 

are classified as either the dominant or co-dominant 

species in 150 forest and shrubland communities 

(NatureServe Explorer, 2014, see below). In some 

wetlands, species such as Fraxinus nigra Marshall 

(black ash) (Figs. 8, 10) and Fraxinus profunda 

(Bush) Bush (pumpkin ash) (Figs. 7, 9) form almost 

pure monocultures that are highly susceptible to 

EAB (Tardif and Bergeron, 1992; Rebek et al., 2008; 

Klooster et al., 2014; NatureServe Explorer, 2014; Jim 

McCormac and Jim Bissell pers. comms). Laboratory 

trials suggest that all 16 species of North American 

Fraxinus may be suitable hosts for larval development 

of EAB and thus are susceptible to attack (Anulewicz 

et al., 2008; Leah Bauer pers. comm, Deb McCullough 

pers. comm). Even small-stemmed western species 

have the potential to support the beetle given that 

saplings of white and green ash as narrow as 1 cm in 

diameter are exploited by the beetle and its immature 

stages in the eastern United States. Once infested, tree 

death typically follows within 2 to 6 years (Knight et al., 

2013). In addition, the related (olive family) fringetree 

(Chionanthus virginicus L.) is also susceptible to attack, 

but the beetle’s impact on that host is as yet unstudied 

(Entomology Today, 2014). 

Climate models for the beetle and projections 

for its spread are still in development and burdened 

with considerable uncertainty (Sobek-Swant et al., 

2012; Liang and Fei, 2014), thus it is impossible 

to know how far north, south, and west the beetle 

might spread in North America and which Fraxinus 

populations are most at risk. Consequently, for the 

purposes of this assessment, we consider the entirety 

of the North American ash flora to be vulnerable. 

We first examine the forest community types where 

ash is a dominant or co-dominant and then provide 

a brief assessment for each of the sixteen Fraxinus 

that grow north of Mexico. Each treatment includes 

a synopsis of a species’ habitat, range, conservation 

status, known susceptibility to EAB, and a summary 

of its specialist herbivores. We then include a brief 

discussion of the importance of ash to vertebrate 

wildlife before addressing the core of our contribution 

– a comprehensive evaluation of the invertebrate 

herbivore fauna of North American Fraxinus 

likely to be threatened by the spread of EAB. Our 

evaluation is constructed from reviews of literature, 

correspondence with taxonomic authorities, and 

DLW’s 30-year rearing program. We ignore generalist 

herbivores known to feed on ash, although a few 

oligophagous species are discussed. 

Our assessment is novel in that we considered 

feeding records in older and derivative literature 

as unconfirmed, given the large number of 

misattributed records plaguing recent compendia and 

risk-assessment literature. Instead, we adopted an 

authority-driven approach whereby we contacted one 

or more active systematists or experts for taxa known 

to have specialist herbivores on woody plant taxa. We 

received information from more than 80 taxonomic 

authorities with first-hand knowledge of appropriate 

literature, species-level taxonomy, life history data, 

and ecological associations. Compared to previous 

assessments, our approach yielded a dramatically 

different list of potentially imperiled herbivores, 

essentially half of which are newly reported here. 

Our work includes a revised set of risk rankings for 

98 species that we believe to be threatened by the 

emerald ash borer. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

17 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

5 6 7 

8 9 

10 11 

Figures 5-11. Ash trees and ash-dominated communities: (5) Google Earth view of black ash swamp west of Lincoln, Wisconsin; 

Fraxinus nigra is dominant over thousands of hectares of this boreal wetland; (6) Majestic blue ash (F. quandrangulata) tree 

near Lexington, Kentucky. (Photo courtesy Daniel Boone); (7) Vernal pool with canopy of pumpkin ash (F. profunda), Momence 

Wetlands Land and Water Reserve, Illinois; note buttress roots or knees which help the trees uptake oxygen when the pool is 

inundated. (Photo courtesy Judy Semroc); (8) Black ash dominated swamp near Black Lake, Michigan. (Photo courtesy Anton 

Reznicek); (9) Vernal pool near Astabula, Ohio with pumpkin ash as the dominant canopy tree; the dry vernal pool shown here is 

a breeding area for mole salamanders. (Photo courtesy Judy Semroc)—see Effects to Vertebrates; (10) Northern hardwood swamp 

dominated by black ash near Wallon Lake, Michigan. (Photo courtesy Anton Reznicek); (11) Upland hickory-white ash glade (F. 

americana) in Litchfield County, Connecticut. (Photo courtesy Ken Metzler) 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

18 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

methods and rationale 

To determine ecological impacts of EAB infestations 

on communities, we contacted 20 people with 

first-hand experience (botanists, reserve managers, 

Department of Natural Resources (DNR) ecologists, 

State Nature Conservancy chapters, forest managers, 

land managers, seasoned naturalists, wildlife 

biologists, and especially those with extensive field 

experience) in the forests and woodlands where EAB 

has been resident for four or more years (Appendix 

1). We focused our surveys and correspondence on 

three states and one province with conspicuous EAB 

impacts: Michigan, northern Ohio, northeastern 

Indiana, and southwestern Ontario. For each state 

or province we initially contacted a lead biologist in 

the DNR (or its functional equivalent) and a state or 

provincial office for The Nature Conservancy and 

then made efforts to approach additional state or 

provincial authorities that had been endorsed for 

their knowledge of the impacts of EAB. Vertebrate 

biologists that we contacted for information on the 

ecological (especially dietary) importance of Fraxinus 

are listed in Appendix 1. Conversations with Anton 

Reznicek (University of Michigan), renowned Great 

Lakes Region botanist, Jim Bissell (Cleveland Museum 

of Natural Science), and Jim McCormac (Ohio 

Division of Wildlife) carried special force. 

To identify and assess imperilment of plant 

communities containing ash, we used the U.S. 

National Vegetation Classification (USNVC) revised 

in 2008 and subsequently developed by NatureServe 

Explorer and state Heritage Programs (NatureServe 

Explorer, 2014). The classification system for 

the North America’s plant community types – a 

jurisdictional subset of the International Vegetation 

Classification – is a spatially extensive, range-wide, 

on-going collaboration of federal, international, 

academic, and state partners, housed and managed 

by NatureServe. Our treatment focuses on ecological 

communities recognized at the Group level in the 

International Vegetation Classification system and 

tallies the biological communities in which any one 

of North America’s 16 Fraxinus species is named as a 

dominant or co-dominant plant species. We capitalize 

Group when the word is meant to convey rank in the 

USNVC classification. 

Ash specialists were defined as those species for 

which Fraxinus was deemed a principal larval or 

adult host. Stated differently, specialists are those taxa 

that would be expected to be severely compromised 

were Fraxinus eliminated from the taxon’s range. 

We excluded more than 180 ash-feeding herbivores 

that are known to feed on hosts outside the family 

Oleaceae (Gandhi and Herms, 2010; Robinson et 

al., 2014). Host records were verified by contacting 

principal taxonomic experts (listed with affiliations 

in Appendix 2). Frequently, multiple experts, with 

differing regional data or taxonomic knowledge, were 

consulted for the same taxon. We were not able to 

make contact with an active North American thrips 

(Thysanoptera) systematist and caution that much 

remains to be learned about North America’s mite 

fauna. Documentation for all taxa and the listed hosts 

is given in the References column and, as appropriate, 

in the Comments column of Table 4. Conversations 

are referenced as “pers. comm.” and letters and emails 

are referenced as “in litt.” 

We use the term polyphagous to refer to cases 

where herbivores feed on members of more than 

two families, oligophagous to refer to cases where 

the herbivores feed on more than one genus in 

the Oleaceae, and specialist to refer to cases where 

Fraxinus is the sole or principal host in nature1

. We 

restrict use of monophagous to those instances where 

only a single species is (known to be) consumed, 

and ecological monophagy to instances where a 

species’ diet is restricted to a single member of 

the Oleaceae because only one host species grows 

in a given geographic location; presumably the 

herbivore would use other congeners (Fraxinus) or 

perhaps confamilials (Oleaceae) were these available. 

Throughout this paper, our diet-breadth assessment 

of invertebrates applies to the most specialized life 

stage; thus, if a leaf beetle eats just Fraxinus as a larva 

but browses on a spectrum of plants as an adult, our 

discussion and risk assessment is based on the larval 

stage. 

1

This is more restrictive than most insect-plant literature, where 

oligophagous refers to herbivores that consume plants from 

just 2-3 families and polyphagous is used to refer to herbivores 

consuming four or more families. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

19 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

We follow Hinsinger et al. (2013) in recognizing 

four Sections of Fraxinus in North America. Section 

is capitalized when the word is meant to convey 

nomenclatural rank (and phylogenetic membership), 

i.e., roughly equivalent to a subgenus. Authors for 

scientific names of imperiled arthropods are given 

in Table 4; author names for arthropod species not 

treated in Table 4 are given in the text the first time 

that taxon is discussed. Arthropod family names are 

given in the text and Table 4 except where family 

membership has been made obvious by accompanying 

text. Authors for Fraxinus species appear in the section 

entitled North America’s Sixteen Fraxinus. 

Species-level taxa (n = 98) were assigned an 

imperilment or risk category after we had verified host 

records for each. Four categories of risk were adopted: 

Very High, High, Moderate, and Low, with all examples 

of the latter excluded from this work. If only Fraxinus 

and native Chionanthus L. (fringetree) species were 

among the reliably reported hosts, individuals were 

given a High risk rating. If additional Oleaceae hosts 

were recorded, we assigned risk ratings in the follow 

manner: herbivores known to include Forestiera Poir. 

(swamp privet or desert olive) species were regarded 

as Moderate risk species because native Forestiera 

are abundant enough to serve as an alternative host 

to Fraxinus; ash-feeding and fringetree-feeding 

herbivores also reported from non-native Oleaceae 

hosts, e.g., Olea L. (olive), Ligustrum L. (privet), 

and Syringa L. (lilac) were given a High to Moderate 

risk rating as these hosts are either considered not 

abundant enough in wildlands or too infrequently 

used to serve as viable (sole) hosts for these taxa over 

extended time periods were ash to be functionally 

eliminated. If a species was believed to have a strong 

preference for Fraxinus over other Oleaceae, its 

risk rating was increased; conversely, those with a 

preference for Forestiera resulted in a reduced rating. 

One species, Prociphilus americanus (Aphididae), 

was determined as High risk despite feeding on Abies 

Miller (fir) because both Fraxinus and fir are primary 

hosts in different stages of this aphid’s alternating life 

cycle. 

In a few cases where we suspected an apparent 

specialist may prove to be a polyphage, e.g., Banasa 

rolstonii (Pentatomidae), Diaspidiotus fraxini, and 

Diaspis fraxini (both Diaspididae), we invoked the 

precautionary principle and assigned these species 

a High risk rating. Likewise, species in need of 

taxonomic study were still included and generally 

ranked as High; e.g., Sphinx near chersis, Sympistis 

fortis, Hyrdelia near inornata, and Zelleria near 

hepariella. In these cases and others, our thinking is 

conveyed in the Comments section of Table 4. 

Figure 12. Google Earth image of Saint Mary’s River west of Decatur, Ohio. The dead trees in 

this image about the periphery in the riparian corridor east of Rockford are essentially all 

green ash. The red star indicates the approximate location of the stand shown in Figure 1. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

20 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	

	 	 	 	

	 	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	

ECOLOGICAL IMPACTS TO NORTH
 

AMERICAN ASH
 

Flowers et al. (2013) estimate that there are 8.7 billion 

ash trees and saplings in the lower 48 states – making 

up roughly 2.5% of the aboveground forest carbon 

mass in this region. Over most of North America, ash 

trees tend to grow in mixed hardwood woodlands 

and forests and are infrequently an ecologically 

dominant tree at landscape levels. Even in regions 

of the Midwestern United States, where a significant 

portion of all Fraxinus have been killed, we were 

unable to easily detect affected communities using 

Google Earth satellite imagery; although one such 

example – a severely damaged area along the Saint 

Mary’s River, east of Decatur, Ohio – is shown in 

Fig. 12. Another important exception are black ash 

forests, which can be ecologically dominant at larger 

spatial scales; in many northern woodlands, F. nigra 

grows in virtual monocultures over hundreds of 

hectares (see below and Figs. 5, 8, 10). Furthermore, 

over smaller spatial scales, ash species have great 

ecological importance and, by definition, are essential 

elements in the woodlands and forests where they are 

dominant or co-dominant species. The U.S. National 

Vegetation Classification and NatureServe Explorer 

(2014) identify 150 U.S. and Canadian forest and 

shrubland community types where a Fraxinus species 

is named as a dominant or co-dominant element. 

Just four Fraxinus species account for 82% of the 150 

community Groups where ash is regarded to be a key 

community element: green ash (n = 55), white ash (n 

= 43), black ash (n = 14), and Oregon ash, Fraxinus 

latifolia Benth. (n = 12). Likewise, only eight species 

of Fraxinus grow as the (lead) dominant tree species 

in 51 community types: green ash (n = 18 community 

Groups), Oregon ash (n = 10), white ash (n = 8), black 

ash (n = 6), Carolina ash, F. caroliniana Miller (n = 3), 

blue ash, F. quadrangulata Michx. (n = 3), singleleaf 

ash F. anomala (n=2) and pumpkin ash (n = 1). 

Ecological contributions of each of North America’s 

16 native Fraxinus, as identified in the U.S. National 

Vegetation Classification and NatureServe Explorer 

(2014), are summarized in Table 1. 

In Table 2 we list 16 North American forest 

community types where a Fraxinus is the dominant 

tree and the assemblage is regarded as either critically 

imperiled (G1) or imperiled (G2) in NatureServe 

Explorer (2014). Most of these imperiled forest types 

occur south of Pennsylvania; three are restricted to 

Oregon and Washington. Fortunately, none occur in 

the most severely affected areas of the Midwestern 

United States. 

A few community types warrant special mention 

because of their spatial extent or because of their 

vulnerability. In Wisconsin and elsewhere, swamps 

with black ash as the sole dominant canopy species 

may encompass >1000 ha (Fig. 5). Palik et al. (2012) 

speculated that many such black ash swamps, should 

ash disappear, may change permanently to shrublands 

as no other tree species exists in large enough 

concentrations to form a new canopy. Similarly, along 

the Atlantic Coastal Plain, Carolina ash sometimes 

accounts for much of the above-ground biomass in 

bottomlands and wetlands. 

The most significant ecological impacts of EAB

to woodlands and forests will be determined by what

plant associations establish post-invasion (Flowers et

al., 2013; Knight et al., 2013; Burr and McCullough,

2014). Future projections for communities formerly

dominated by ash are still a matter of conjecture

because no EAB infestations, with their concomitant

ecological consequences, have run full course.

Undoubtedly, there will be taxonomic variation in

which species replace ash due to differences in soil

type, hydrology, light, seed banks, and the local pools

of potential colonists. In the vicinity of Ann Arbor,

Michigan – where EAB was first documented – the

ecological vacuum created by the loss of green ash

has been filled by spicebush (Lindera benzoin L.),

pawpaw (Asimina triloba Dunal), and prickly ash

(Zanthoxylum americanum Mill.). In the same area,

one wetland formerly dominated by black ash has

changed into a monoculture of sedge (Carex L.).

While both ash habitats changed structurally, neither

gave way to invasive species (Anton Reznicek,

pers. comm). In Indiana and Ohio, silky (Cornus 

amomum Mill.) and gray dogwoods (C. racemosa 

Lam.) have flourished in communities where ashes

(mostly green and black) have been lost (Jim

Bissell, Mike Homoya, and Jim McCormac, all

pers. comm). Invasive shrubs that have increased
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

21 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

	 	 	 	 	 	 	

	 	 	 	 	

	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	

 

in post-EAB woodlands and bottomlands in Indiana

and Ohio include multiflora rose (Rosa multiflora 

Thunb.), honeysuckle (Lonicera morrowii A. Gray

and three other honeysuckles), and glossy buckthorn

(Rhamnus alnifolia L’Hér), but not to the extent that

many feared. As noted above, even in southeastern

Michigan where EAB was first documented, it is still

too early to know what the ecological consequences of

ash decline will be. Over time, sedge meadows, reed

canary grass (Phalaris arundinacea L.) bottomlands,

and various shrublands that arise following ash

die-off will give way to forest communities, but the

composition of these replacement forests remains to

be seen. It is also too soon to disregard Fraxinus as an

eventual component of replacement forests as virtually

all EAB-affected communities in the Midwestern

United States have seedling and sapling ash recruiting

presently (Anton Reznicek pers. comm). If native and

introduced natural enemies (e.g., Duan et al., 2013;

also see Chapters 8 and 9) are able to reduce emerald

ash borer density, Fraxinus could regain some of its

former ecological importance.

Where significant physiognomic changes occur, 

e.g., where a woodland is initially replaced by a 

graminoid wetland or shrubland, the biota, species 

interactions, hydrology (Slesak et al., 2014), light 

regimen, nutrient cycling, vertebrate food value, and 

other core ecosystem characteristics will be altered. 

Beyond the obvious loss of ash-specialized herbivores, 

structural changes in affected woodlands may change 

a forest’s suitability as breeding habitat and cover 

for resident vertebrates and invertebrates (e.g., see 

discussion of mole salamanders [Ambystoma species] 

in pumpkin ash swamps later in this chapter). On a 

smaller spatial scale, all of the above applies to the 

forest gaps that form when stands or glades of ash are 

killed by EAB. Such canopy gaps are noted to cause 

microclimate effects altering, among other biota, 

ground beetle populations (Gandhi et al., 2014). These 

gaps also open up forests for invasions by plant species 

normally limited by light availability (Herms and 

McCullough, 2014). 

When native plants are replaced by exotic species, 

such as glossy buckthorn and exotic honeysuckles in 

Indiana and Ohio (see above), there can be cascading 

consequences to higher trophic levels. Exotic plants 

often carry lower herbivore loads (Tallamy and 

Shropshire, 2009) and as a consequence would not 

support as many insectivorous birds, mammals, or 

other wildlife. However, we are compelled to interject 

here that we generally find ash to be relatively 

herbivore free. Low insect/pest loading is one reason 

that ashes are often chosen for city plantings (see 

species treatments in Elias [1987]). In Tallamy and 

Shropshire (2009)’s compilation of the Lepidoptera 

feeding on 1385 plant genera grown in the MidAtlantic States, Fraxinus ranks sixteenth in richness. 

Green and white ash trees planted in cities, towns, and 

parks in the western United States show little evidence 

of herbivory (DLW pers. observation). Likewise, in 

European woodlands, ash trees have been documented 

to have low herbivore loads relative to many other 

genera of forest trees (Fischbacher et al., 1998). Among 

four tree genera surveyed near Basel, Switzerland 

(Carpinus L. [hornbeams], Fagus L. [beech], Fraxinus 

L. [ash], and Quercus L. [oak]), ash yielded only about 

half the caterpillar frass observed on other surveyed 

genera. Moreover, while invasive plants generally have 

depauperate herbivore loads, at least Lonicera and 

Rhamnus produce abundant fruits that are exploited 

by a range of birds and other vertebrates. As with all 

ecological change, some species will benefit, and others 

will suffer. 

A final note, brought to our attention by Anton 

Reznicek, is that considerable demographic differences 

exist among North American Fraxinus as to their 

age and size of first reproduction. Green ash begins 

flowering and fruiting as a young tree – at diameters 

frequently ignored by EAB, and thus the species has 

the potential to persist as young trees, e.g., in open 

riparian and floodplain communities. By contrast, 

white and pumpkin ash fruit later, and typically young 

trees will succumb to EAB infestation before they 

can bear seed. Hence these species’ fate and those of 

their dependent herbivore faunas are likely to differ 

substantially from those of green ash. 

NORTH AMERICA’S SIXTEEN FRAXINUS 

Below we provide a synopsis addressing the range, 

preferred habitat, ecological importance, known 

susceptibility to EAB, and herbivore specialists of 
 

22 

BIOLOGY AND CONTROL OF EMERALD ASH BORER Table1 . Native ash species found North of Mexico with their USNVC/NatureServe importance and tally of specialist herbivore fauna. Specialist Herbivores Forest Community 
 Group
 

CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 411746129

20

31231

1010 

Acari
 

Coleoptera
 

Diptera
 

Hemiptera
 

Hymenoptera
 

Lepidoptera
 

Total Species Clade Species Common Name 

Dominant 


Co-dominate
 

Total
 Approx. Region 

Dipetalae Fraxinus dipetala California Ash 1 

Melioides Fraxinus cuspidata Fragrant Ash 

136

1243

5

55

5292

14

1 

West Southwest 

1 1 2 

Fraxinus anomala Singleleaf Ash 2 1 Southwest Fraxinus quadrangulata Blue Ash 3 3 East 1 

Fraxinus latifolia Oregon Ash 10 2 West 2 4 4 2 5 Fraxinus papillosa Chihuahuan ash South Fraxinus americana White Ash 8 35 Midwest/East 2 11 6 9 3 15 Fraxinus profunda Pumpkin Ash 1 4 East 1 Fraxinus pennsylvanica Green Ash 18 37 Midwest/East 1 6 4 6 1 11 Fraxinus velutina Velvet Ash 5 Southwest 2 5 8 5 

Fraxinus berlandieriana Mexican Ash 2 Texas 3 Fraxinus caroliniana Carolina Ash 3 6 Southeast 1 

Fraxinus albicans Texas Ash 2 Texas 1 1 

Pauciflorae Fraxinus greggii Gregg’s Ash Texas 2 

Fraxinus gooddingii Goodding’s Ash Arizona 1 

Fraxinus Fraxinus nigra Black Ash 6 8 Midwest/Northeast 1 1 1 7 

NA Fraxinus spp. various ashes 1 East 1 1 1 5 2 Footnote: In-the-wild host ranges are poorly known for most of the arthropod species in this table. We suspect that virtually all of the taxa that appear to be specialized in this table, in fact, have broader host ranges than indicated above due to undersampling—see Feeding Guilds and Specificity of Arthropod Herbivores discussion. Diets of southern and western taxa are especially poorly known. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

23 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Table 2. Sixteen globally imperiled forest communities dominated by Fraxinus. See NatureServe Explorer (2014) for details on distribution, ranking, and additional plant 

associations.

Ecological Community dominated by Fraxinus sp. Fraxinus americana / Andropogon gerardii - Sorghastrum nutans - Schizachyrium scoparium -Pycnanthemum tenuifolium Herbaceous Vegetation 

Fraxinus americana - Juniperus virginiana / Talinum teretifolium - Polygonum tenue -

Opuntia humifusa Wooded Herbaceous Vegetation Fraxinus americana / Physocarpus opulifolius / Carex pensylvanica - Allium cernuum -

(Phacelia dubia) Wooded Herbaceous Vegetation Fraxinus americana - Carya glabra / Symphoricarpos orbiculatus - Rhus aromatica / Piptochaetium

avenaceum Woodland Fraxinus americana - Carya ovata / Frangula caroliniana / Helianthus hirsutus Woodland 

Fraxinus americana - Carya glabra / Muhlenbergia sobolifera - Helianthus divaricatus - Solidago 

ulmifolia Woodland Fraxinus americana - Juglans nigra - Ulmus rubra / Acer barbatum - Ostrya virginiana / Ptelea trifoliata Forest Fraxinus latifolia / Carex deweyana - Urtica dioica Forest Fraxinus latifolia / Juncus patens Forest Fraxinus latifolia - Populus balsamifera ssp. trichocarpa / Rubus spectabilis Forest Fraxinus nigra - Abies balsamea / Rhamnus alnifolia Forest Fraxinus pennsylvanica - (Ulmus americana) - Pinus taeda / Morella cerifera - Juniperus virginianavar. silicicola Tidal Forest Fraxinus pennsylvanica - (Carya aquatica) / Forestiera acuminata / Phanopyrum gymnocarponDepression Forest Fraxinus pennsylvanica - Populus heterophylla - Ulmus americana - (Quercus texana) Forest Fraxinus quadrangulata - Juniperus virginiana var. virginiana / Schizachyrium scoparium - Lithospermum canescens Woodland Fraxinus quadrangulata - Quercus macrocarpa - Quercus muehlenbergii / Arundinaria gigantea ssp. gigantea / Elymus spp. Woodland 

NatureServe Status Critically imperiled Critically imperiled Imperiled Imperiled Critically imperiled? Imperiled Imperiled Critically imperiled Imperiled Imperiled Critically imperiled Critically imperiled - Imperiled Imperiled? Imperiled? Imperiled Critically imperiled? 

Distribution* 

MD, VA 

VAVA

GA, NC 

VA

MD, VA, WV 

AL?, FL, GA?

OR, WA 

OR

OR, WA? 

PA?, WV 

NC

TX

AR?, LA 

KYKY 

Division Eastern North American Dune & Coastal Grassland & ShrublandEastern North American Grassland, Meadow & ShrublandEastern North American Grassland, Meadow & ShrublandEastern North American Cool Temperate Forest Eastern North American Cool Temperate ForestEastern North American Cool Temperate ForestSoutheastern NorthAmerican Warm Temperate ForestVancouverian Flooded & Swamp Forest Vancouverian Flooded & Swamp Forest Vancouverian Flooded & Swamp Forest Eastern North American Flooded & Swamp ForestEastern North American Flooded & Swamp Forest Southeastern NorthAmerican Flooded & Swamp Forest Southeastern NorthAmerican Flooded & Swamp Forest Eastern North American Cool Temperate ForestEastern North American Cool Temperate Forest 

* AL - Alabama, AR - Arkansas; FL - Florida; GA - Georgia; KY - Kentucky; LA - Louisiana; MD - Maryland; NC - North Carolina; OR - Oregon; PA - Pennsylvania; TX - Texas; VA - 

Virginia; WA - Washington; WV - West Virginia 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

24 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

each North American Fraxinus. We group ash species 

by four phylogenetic sections based on Hinsinger 

et al. (2013), beginning with the nominate Section 

Fraxinus, which is monotypic in the Americas and 

represented only by black ash (F. nigra). Of these 

four phylogenetic groupings, Section Melioides 

(in its broad sense) contains the most ecologically 

important, widespread species of ash; it is also the 

most speciose section, with 10 North American 

species. For the purposes of our evaluation, we make 

the assumption that all 16 North American species 

are vulnerable to the emerald ash borer, given initial 

host preference studies and the uncertainty in climate 

niche models for the insect (Sobek-Swant et al., 2012; 

Liang and Fei, 2014). However, it seems unlikely to 

us that the beetle will pose a major threat to the nine 

species of western arid land ash (F. albicans Buckley, 

F. anomala Torr. ex S. Watson, F. berlandieriana 

DC., F. cuspidata Torr., F. dipetala Hook. & Arn., F. 

gooddingii Little, F. greggii, F. papillosa Lingelsh, and 

F. velutina Torr.), given that EAB does not inhabit 

xeric and desert areas in its native range. 

Section Fraxinus 

Black ash. Fraxinus nigra, a small tree that is the 

most northern member of its genus, is distributed 

across southern Canada from eastern Manitoba to 

Newfoundland, south in mountains through West 

Virginia, in the Ohio River Valley to southern Indiana 

and Illinois, and in much of Iowa (Elias, 1987). Black 

ash is a major component of 14 forest community 

Groups (NatureServe Explorer, 2014): six as a 

dominant tree species and eight as a co-dominate. It 

is the dominant tree in one critically imperiled (G1) 

forest community type, the Fraxinus nigra - Abies 

balsamea /Rhamnus alnifolia forests of West Virginia 

and Pennsylvania – two states with established EAB 

populations. 

Black ash grows in damp woods, bottomlands, 

swamps, and other wetlands; it tolerates considerable 

inundation (Fig. 8). Common associates include 

black spruce (Picea mariana [Mill.] Britton, Sterns 

& Poggenb.), white cedar (Thuja occidentalis L.), 

tamarack (Larix laricina [Du Roi] K. Koch), birch 

(Betula L.), and especially red maple (Acer rubrum 

L.). It sometimes grows in nearly pure stands over 

hundreds of hectares, principally in the North 

American Great Lakes region (Fig. 5). Red mapleblack ash swamps cover thousands of hectares in 

southern Canada and the northern United States. 

Where Fraxinus nigra grows in monocultures or as 

a dominant in either the canopy or subcanopy, the 

emerald ash borer represents a special threat. Black 

ash is considered to be the most vulnerable North 

American ash species as its range lies within the 

presumed climate niche for the beetle (Klooster et al., 

2014; Liang and Fei, 2014; Leah Bauer pers. comm.). 

Of additional concern is how plant community 

composition will change in black ash stands post-EAB 

invasion. Where the canopies are lost there is added 

risk that the local biota, forest structure, hydrology, 

and other core ecological attributes will be harmed. 

We recorded ten ash specialist herbivores from 

black ash: one aphid, one seed weevil, one sawfly, 

one gracillariid leafminer, two noctuids, one pyralid, 

and three sphingids (Table 4). All but one of these 

arthropods are also known from Section Melioides 

sensu stricto Fraxinus, and especially F. americana, 

F. pennsylvanica, or both. The rarely encountered 

Canadian sphinx (Sphinx canadensis) (Sphingidae) 

warrants special consideration. Tuttle (2007) wrote: 

“In northeastern Indiana, [Sphinx canadensis] is 

closely associated with the understory of dense 

hardwood stands along the perimeter of wetlands. 

Over several seasons larvae were found exclusively on 

black ash (Fraxinus nigra: Oleaeceae), although two 

additional ash species [F. americana, F. pennsylvanica] 

were present. Just as significant, larvae were never 

found on black ashes growing in open areas, 

although those same trees supported the larvae of 

two other sphingid species.” The northern range of 

the Canadian sphinx closely follows that of black ash. 

Southward the moth’s range extends beyond that of 

F. nigra, south of the Ohio River, where the species is 

rare and its Fraxinus hosts are unknown. 

Section Pauciflorae 

Goodding’s ash. Fraxinus gooddingii is a narrowly 

distributed shrubby ash limited to southeastern 

Arizona and northern Sonora. It grows on rocky 

slopes (often on limestone), in desert scrub, oak 

woodlands, and riparian associations, scattered 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

25 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

	 	 	 	 	

	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 	 	 	

	 	 	 	 	 	 	

	 	 	 	 	 	 		

 

among other woody shrubs on lower canyon slopes; 

most records are from arroyos and canyon bottoms 

from 1100 to 1500 meters (SEINet, 2014). 

No previous literature has identified specialist 

herbivores on this host. Jim Verrier and DLW 

found Philtraea elegantaria (Geometridae) feeding 

on Goodding’s ash in Rock Corral Canyon in the 

Tumacácori Range. Sphinx libocedrus (Sphingidae) 

feeds on this ash in Arizona (Tuttle, 2007), but species 

of Forestiera are presumed to be its principal hosts. 

Gregg’s ash. Fraxinus greggii is found in the

Trans-Pecos region of southwestern Texas south

at least to Hidalgo, Mexico. Gregg’s ash is often

limited to riparian corridors in arroyos, canyon

bottoms, and along water courses from 400 to 1800

meters (Powell, 1998; SEINet, 2014). It grows on

cliffs, rocky slopes, and canyon bottoms, frequently

on limestone. Throughout its range, it grows as a

subdominant: typically as scattered plants, in desert

canyons and foothills, usually upslope from water.

Noel McFarland (pers. comm.) found caterpillars 

of Philtraea paucimacula (Geometridae) in high 

densities on Gregg’s ash near Laredo, Texas. Sphinx 

libocedrus (Sphingidae) is known from this ash, as 

well as Forestiera (Table 4). 

Section Melioides 

White ash. Fraxinus americana is the second 

most abundant and widespread native North 

American ash. It is a common component in many 

forest types, including bottomlands, open upslope 

woodlands (Fig. 11), and mixed hardwood forests. 

Typically, white ash occurs in sites with enriched, but 

well drained, moist soils, where it grows in association 

with sugar maple (Acer saccharum Marshall), tulip 

tree (Liriodendron tulipifera L.), cherry (Prunus L.), 

beech, sweet gum (Liquidambar styraciflua L.), red 

maple, and willow (Salix L.). NatureServe Explorer 

(2014) identifies eight ecosystems with white ash as a 

dominant tree and 35 where it is a co-dominant. Of 

the eight forest community Groups where white ash 

is dominant, three are critically imperiled (G1) and 

four are imperiled (G2) (NatureServe Explorer, 2014) 

(Table 2). White ash seeds are eaten by many birds 

and squirrels (Burns and Honkala, 1990) and it is 

commonly planted as shade trees in yards, parks, and 

along streets (Elias, 1987; Burns and Honkala, 1990). 

EAB is thought to prefer other Fraxinus species over 

white ash (Anulewicz et al., 2008), but F. americana is 

still attacked and generally suffers very high mortality. 

However, apparent resistance of white ash to EAB has 

recently been seen in Ohio, with some white ash trees 

surviving in forests where green ash have succumbed 

to the beetle (Jim Bissell pers. comm.). 

White ash has the richest fauna of ash-specialized 

herbivores in North America – three times as many 

as any western ash. We list 46 species in Table 4, but 

suspect that virtually all of the eastern specialists 

listed only from Fraxinus (without an associated 

species epithet) probably use white ash. Specialist 

arthropods feeding on F. americana include 2 mites, 1 

leaf beetle, 5 bark beetles, 4 seed weevils, 1 scarabaeid, 

1 agromyzid, 5 gall midges, 2 aphids, 6 mirids, 1 lace 

bug, 3 sawflies, 2 inchworms, 2 gracillariid miners, 3 

owlets (Noctuidae), 1 pyralid, 1 clearwing borer, and 

5 sphingids (Table 4). Sixteen herbivores are recorded 

only from white ash: 2 Hylesinus (Curculionidae), 

2 Lignyodes (Curculionidae), 1 Xyloryctes 

(Scarabaeidae), 4 Dasineura (Cecidomyiidae), 1 

Prociphilus (Aphididae), 3 Tropidosteptes (Miridae), 1 

Tethida (Tenthredinidae), 1 Hydrelia (Geometridae), 

and 1 Copivaleria (Noctuidae), although none of 

these are known to be strictly monophagous. 

Green ash. Fraxinus pennsylvanica is a smallto-medium-sized, fast growing tree that is the most 

widely distributed ash species in North America, 

extending from southwestern Saskatchewan to Cape 

Breton Island, south to northern Florida and eastern 

Texas. It is an abundant, ecologically important 

species throughout much of this range and thrives 

in floodplains and other bottomlands. Elias (1987) 

notes that F. pennsylvanica is especially abundant 

through the Mississippi Valley. Green ash is the most 

common Fraxinus to grow as a dominant tree in the 

U.S. National Vegetation Classification (USNVC) 

system. Fifty-five ecological community Groups 

contain F. pennsylvanica as a dominant (n = 18) or codominant tree (n = 37) (NatureServe Explorer, 2014). 

Green ash is the dominant tree in three forest Groups 

considered to be Critically Imperiled to Imperiled; 

all three of which are flooded swamp forests in the 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

 

southeastern United States (Table 2). In forests where 

green ash is dominant, Burr and McCullough (2014) 

note that green ash is “unlikely to persist as a dominant 

species” after EAB invasion. Its seeds are an important 

forage for a variety of birds, small mammals, and 

other wildlife; deer and moose (Alces alces L.) feed 

on new growth (Elias, 1987). Its strong wood is sold 

commercially for bats, oars, and tool handles but is not 

as desirable for wood working as white ash (Burns and 

Honkala, 1990). 

We record 29 Fraxinus-Oleaceae specialists from 

green ash; thus, it ranks only behind white ash in 

its importance to Fraxinus-specialist herbivores: 1 

mite, 1 buprestid, 3 bark beetles (Hylesinus), 2 seed 

weevils (Lignyodes), 1 agromyzid, 3 gall midges 

(Cecidomyiidae), 1 aphid, 5 mirids, 1 sawfly, 4 

gracillariid miners, 2 owlets (Noctuidae), 1 pyralid, 

1 clearwing borer (Sesiidae), and 3 sphingids. 

Seven species are recorded only from green ash: 

one undescribed Dasineura (Cecidomyiidae), two 

Tropidosteptes (Miridae), and the two gracillariids 

Marmara basidendroca and Marmara corticola. The last 

two of these, so far as known, are monophages, at least 

at the type locality and surrounding areas of upstate 

New York (Fitzgerald, 1973; Terry Fitzgerald pers. 

comm.). See also Imperilment Risk Rating discussion. 

Mexican ash. Fraxinus berlandieriana is a small 

tree that occurs from the vicinity of Austin, Texas 

southward and westward into Mexico. The core of 

its range is in the Mexican states of Coahuila, Nuevo 

Leon, and Tamaulipas. It grows in moist canyons and 

along streams and rivers of the Rio Grande Plains 

and southern prairies (Vines, 1984) and is frequently 

planted as a shade tree in parks and cities. Two 

community types in Texas include Mexican ash as a codominate (n = 2), one of which is considered critically 

imperiled/imperiled (G1G2) (NatureServe Explorer, 

2014). 

Ash specialists reported from the United States 

include the buprestid Trigonogya reticulaticollis, the 

chrysomelid Capraita sexmaculata, and the seed weevil 

Lignyodes helvolus. While Mexican ash is the only 

reported host for T. reticulaticollis, based on the biology 

of related metallic wood boring beetles, it is probable 

that its host range will be found to include other 

Oleaceae. 

Carolina ash. Fraxinus caroliniana is a small 

tree of the Atlantic Coast Plain from Virginia, south 

through much of Florida, west to east Texas and 

southern Arkansas. It grows in swamps, wetlands, 

bottomlands, and other mesic to wet forest types. 

Like many other members of the genus, it does 

especially well in marl soils (SEINet, 2014). Carolina 

ash commonly grows with gums (Nyssa L.), hollies 

(Ilex L.), sweet gum, sugarberry (Celtis laevigata 

Willdenow), and others (Elias, 1987); it can be 

locally abundant as an understory member of bald 

cypress-tupelo swamps (SEINet, 2014). Fraxinus 

caroliniana is a dominant in nine forest community 

Groups: three as a dominant and six as a co-dominant 

tree (NatureServe Explorer, 2014). It occurs in 

dense monospecific stands in coastal plain areas 

of Louisiana and Texas (in “Fraxinus caroliniana 

Seasonally Flooded Forests”), which are deemed 

G2G3 imperiled-vulnerable communities. Only one 

herbivore, the sphingid moth Ceratomia undulosa, 

an oligophage on Oleaceae, is recorded from this 

Fraxinus. The lack of feeding records for this ash 

is almost certainly an artifact of limited sampling, 

presumably because its preferred habitat is in swamps 

and wetlands and it is not a commercially important 

ash. 

Fragrant ash. Fraxinus cuspidata is a shrub 

(or sometimes small tree) that is found in scattered 

populations across the southwestern United States 

from northwestern Arizona to western Texas and 

south into Mexico, mostly in the foothills of desert 

ranges (SEINet, 2014). It prefers well-drained, rocky 

soils in canyons, and north facing cliffs of limestone, 

sandstone, or igneous soils (Elias, 1987; Powell, 1998; 

SEINet, 2014). It tends to occur in low densities 

intermixed among oaks, leguminous trees, and other 

woody plants. 

Two specialist herbivores have been recorded 

from this small ash: DLW collected caterpillars of 

a Sympistis heterogena (Noctuidae) feeding on new 

spring leaves in May 2014 and a second unidentified 

noctuid2

 species in July of 2014. 

Oregon ash. Fraxinus latifolia is a Pacific 

Coast tree that grows from the Olympia area in 

2

 The caterpillar, seen in late July, was banded with smoky red in 

the early instars and is a new foliage specialist. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

27 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

western Washington south to the San Francisco 

Bay Area (California) and southern Sierra Nevada, 

as well as in disjunct populations in southern 

California’s mountains. The tree grows in “moist 

rich soils along streams and rivers, and in canyons” 

to 500 meters (Elias, 1987). It is an abundant and 

ecologically important tree along riparian corridors 

throughout much of its range, and is the only 

commercially important Fraxinus in western North 

America. Oregon ash is a dominant tree in ten forest 

community Groups and a co-dominant in two others. 

While it will grow in monocultures, at least along 

streams and in floodplains, it more typically grows in 

mixed hardwood stands with maple, alder (Alnus 

Mill.), poplar (Populus L.), and willow; Elias (1987) 

also adds California laurel (Umbellularia californica 

[Hook. & Arn.] Nutt.) and grand fir (Abies grandis 

[Douglas ex D. Don] Lindley) as associates of F. 

latifolia. Three forest communities in the Pacific 

Northwest dominated by Oregon ash are regarded 

as critically imperiled/imperiled in NatureServe 

Explorer (2014) (See Table 2). 

We record 17 species of ash specialists from 

Oregon ash, many for the first time: 2 mites, 2 

bark beetles, 2 seed weevils, 1 aphid, 2 mirids, 1 

tingid, 2 sawflies, and 1 inchworm (Geometridae), 

1 gracillariid leafminer, 1 owlet moth, and 1 ermine 

moth (Yponomeutidae). Five of these are only known 

from Oregon ash: Hylesinus oregonus (Curculionidae: 

Scolytinae); Lignyodes auratus (Curculionidae: 

Curculioninae); Philtraea latifoliae (Geometridae), 

Caloptilia n. sp. (Gracillariidae), and Sympistis fortis 

(Noctuidae). We suspect that their strict monophagy 

is either an artifact of undersampling or because 

Fraxinus specialists whose ranges are restricted 

to the Sierra and areas north of San Francisco are 

monophagous simply because F. latifolia is the only 

ash that grows where they occur. 

Chihuahua ash. Fraxinus papillosa is a 

geographically restricted ash that grows to become a 

small tree. It is found in small populations through 

desert ranges of southeast Arizona, southwestern 

New Mexico, the Chinati Mountains of west Texas, 

and southward into the Sierra Madre Occidental 

Mountains of Mexico (Elias, 1987; Powell, 1998). 

Typically F. papillosa grows in canyon bottoms and 

on north-facing cliffs (SEINet, 2014). Like other 

desert ashes, it occurs as scattered plants in woody 

associations near water or in microhabitats with 

reduced moisture stress. No ash specialists are 

currently recorded on F. papillosa. In Hinsinger et 

al.’s (2013) study, Chihuahuan ash grouped with 

Oregon ash (F. latifolia), in a clade outside of all other 

members of the Melioides sensu stricto section of the 

genus. Because of this phylogenetic difference and 

its taxonomic and geographic isolation, Chihuahuan 

ash strikes us as a likely candidate for hosting unique 

herbivores. 

Pumpkin ash. Fraxinus profunda grows in 

scattered locations across eastern North America, with 

most occurrences along the Atlantic Coastal Plain and 

through the Ohio and Mississippi River Valleys. It is 

restricted to very wet soils that include bottomlands, 

floodplains, swamps (especially bald cypress and tupelo 

swamps), and coastal marshes (Elias, 1987; Burns and 

Honkala, 1990; Nesom, 2010) (Figs. 7, 9). Fraxinus 

profunda is a dominant (n = 1) and co-dominant (n = 

4) in five eastern forest community types, one of which 

is imperiled (NatureServe Explorer, 2014). This ash 

species is quite susceptible to EAB; devastated would 

not be an overstated descriptor for some local Ohio 

preserves where pumpkin ash once grew as a dominant 

species (Jim Bissell pers. comm.) 

Only one arthropod species is recorded from F. 

profunda: a mite that is not a specialist on pumpkin 

ash (Table 1). No doubt pumpkin ash’s poorly sampled 

herbivore fauna is a reflection of the difficulty involved 

with sampling the inundated wetlands where this 

tree thrives. Certainly it is a candidate for more study, 

especially given its susceptibility and because its range 

falls entirely within the predicted climatic niche of 

EAB. 

Velvet ash. Fraxinus velutina is a small ash of the 

southwestern United States and northwestern Mexico. 

Its U. S. range is concentrated in Arizona and extends 

westward through arid portions of southern California, 

Nevada, Utah, and eastward into the Trans-Pecos 

region of Texas. It grows near streams, rivers, washes, 

and other areas of reduced moisture stress. Common 

associates include hackberry (Celtis occidentalis L.), 

oak, poplar, sycamore (Platanus L.), and willow. It 

reaches greatest importance in mesic stretches of 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

28 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

canyons between 1200 and 1600 meters where it “can 

form almost pure stands” (Elias, 1987). Velvet ash is 

listed as a co-dominant tree in five forest community 

Groups in NatureServe Explorer (2014). 

We record 20 ash specialist herbivores from 

velvet ash, the third most of any Fraxinus species 

and the greatest number for any western species: 2 

mites, 1 bark beetle, 2 seed weevils, 2 scarab beetles, 

2 aphids, 2 scale insects, 2 plant bugs, 1 stink big, 1 

lace bug, 2 owlet moths (Noctuidae), and 3 sphingids. 

Most of these are known only from F. velutina: the 

mite Brevipalpus cardinalis (Tenuipalpidae), the 

weevil Lignyodes arizonicus (Curculionidae), the 

beetles Dynastes granti and Xyloryctes thestalus (both 

Scarabaeidae), the armored scales Diaspidiotus fraxini 

and Diaspis fraxini (both Diaspididae), the plant 

bug Tropidosteptes illitus (Miridae), the stink bug B. 

rolstoni (Pentatomidae), and the moths Chloronycta 

tybo and Sympistis punctilinea (both Noctuidae) 

and Ceratomia sonorensis and Sphinx near chersis 

(both Sphingidae). In the Sonoran and Chihuahuan 

deserts of the western United States, velvet ash is 

the only Fraxinus considered to be an ecologically 

dominant or, more commonly, co-dominant species. 

Consequently, the loss of velvet ash would have an 

impact on all southwestern Fraxinus herbivores, given 

that it accounts for most of the ash biomass in the 

southwestern United States. 

Section Dipetalae 

Singleleaf ash. Fraxinus anomala is a shrub or 

small spreading tree that grows in canyons, desert 

drainages, washes, and along water bodies of the 

North American Great Basin region. It exists as 

scattered stands in western Colorado, Utah (where it 

is widespread), southern Nevada, and southeastern 

California, central and northern Arizona, and 

extreme northwestern New Mexico (SEINet, 2014). 

Fraxinus anomala is a common riparian element 

between 600-1,900 meters. NatureServe Explorer 

(2014) recognizes singleleaf ash as a dominant (n 

= 2) or co-dominant (n = 1) in three southwestern 

plant community associations (all three are currently 

unranked or unrankable due to lack of data). We do 

not know of any specialist ash herbivores from F. 

anomala, although we suspect that it is the primary 

host for Philatraea utahensis Buckett. 

California or two-petal ash. Fraxinus dipetala 

is a shrubby ash that grows in scattered populations 

in central and southern California’s coastal ranges 

and the foothills of the Sierra Nevada Mountains. It 

thrives either on slightly acidic granite slopes, often 

near watercourses, or on slightly alkaline clays in 

chaparral associations. Below 500 meters, it is usually 

restricted to the upslope vicinities of washes and 

watercourses. Above this, California ash occurs in 

chaparral and other foothill communities, typically as 

a scattered element growing with Pinus L. (pine), oak, 

Arctostaphylos Adans. (manzanita), and others (Elias, 

1987; SEINet, 2014). Fraxinus dipetala is listed as a 

co-dominant (along with Prunus ilicifolia [Nutt. ex 

Hook. & Arn.] Walp.) in one U.S. forest community 

Group by NatureServe Explorer (2014). 

The herbivore fauna of California ash is not well 

known – the plant is easily overlooked, and rarely 

common. Four ash-specialist herbivores are recorded 

from California ash: 1 mite, 1 aphid, 1 inchworm 

(Geometridae), and 1 ermine moth (Yponomeutidae). 

Two moths are known exclusively from this ash: 

Philtraea surcaliforniae (Geometridae) and Zelleria 

near semitincta (Yponomeutidae) (Buckett, 1970) 

(Table 4). 

Blue ash. Fraxinus quadrangulata is a small to 

large tree (Fig. 6) whose core distribution is in the 

Midwestern United States from eastern Kansas to 

extreme southern Ontario, south into Arkansas 

and northern Alabama. Blue ash grows in upland 

woods and on slopes usually over limestone, 

but also in moist woodlands and evidently even 

bottomland forests (Elias, 1987). Typically it occurs 

as a subdominant species (n = 3) intermixed in 

stands dominated by oak, mockernut hickory (Carya 

tomentosa Sarg.), sweet gum, and others. It is listed 

as the dominant tree species in three Kentucky forest 

community types (NatureServe Explorer, 2014): 

critically imperiled (G1) blue ash-oak savannah 

woodlands (Bryant et al., 1980; NatureServe Explorer, 

2014); imperiled (G2) blue ash - eastern red-cedar 

/ little bluestem - hoary puccoon woodlands; 

and possibly no longer extant (GH) Fraxinus 

quadrangulata - Quercus macrocarpa / Arundinaria 

gigantea ssp. gigantea wooded shrublands. Fraxinus 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

quadrangulata is believed to be the most EABresistant Fraxinus in eastern North America and, 

consequently, its relative abundance may increase 

in woodlands and forests where other ash succumb 

to the beetle (Anulewicz et al., 2007; Tanis and 

McCullough, 2012). 

Blue ash has a surprisingly modest herbivore 

fauna. Only one ash specialist is recorded from this 

ash, the moth Plagodis kuetzingi (Geometridae), 

which also occurs on F. americana and presumably 

other ashes. Robinson et al. (2014) lists only two 

generalist Lepidoptera for blue ash. Its diminished 

herbivore fauna no doubt is a reflection of its 

taxonomic isolation: it is the only member of 

the Dipetalae Section in eastern North America 

(Hinsinger et al., 2013). Given the above, perhaps it is 

not surprising that blue ash is more resistant to EAB 

than other eastern members of the genus. Given that 

it represents a unique taxonomic entity in eastern 

North America, blue ash is a candidate for a focused 

herbivore survey, especially for cecidomyiids, leaf or 

bast miners, and other herbivores known to show 

extreme monophagy. 

Texas ash. Fraxinus albicans (= F. texensis) is 

a small drought-tolerant relative of white ash that 

grows on limestone from the Arbuckle Mountains of 

southern Oklahoma southward across the Edwards 

Plateau into south central Texas (Vines, 1984; Elias, 

1987). It is a co-dominant (with oak) in two forest 

community types (NatureServe Explorer, 2014). We 

know of only two reports of specialist herbivores 

from Texas ash: 1 mite and 1 weevil, neither of which 

is monophagous on F. albicans. Robinson et al. (2014) 

does not list any lepidopterans from Texas ash. 

The dearth of feeding records for this ash is surely 

a reflection of its limited geographic distribution 

and thus a sampling artifact. Presumably because 

of its close relation to F. americana (Vines, 1984), 

F. caroliniana, and other members of the Melioides 

sensu stricto section of the genus (Hinsinger et 

al., 2013), F. albicans will be found to share many 

herbivores with other Fraxinus. 

EFFECTS ON VERTEBRATES
 

Martin et al. (1951) regarded North American ashes 

to be “only of moderate importance to wildlife.” 

No vertebrates are monophagous or otherwise 

exclusively dependent on ash or ash-dominated 

communities, although some local populations might 

be energetically or ecologically dependent on ash 

simply due to the fact that Fraxinus are the dominant 

or co-dominant trees in the woodland or forest types 

where they live (northern black ash swamps provide 

compelling examples of such) (Fig. 5). A summary 

of vertebrates using ash as a food source is given in 

Table 3, with the proviso that the published literature 

is greatly biased towards game species. We also note 

that the literature for vertebrates is largely qualitative, 

with little data on the importance of ash relative to 

other food resources; we suspect that the paucity of 

studies addressing the ecological importance of ash 

may be a reflection of the fact that, by itself, ash trees 

rarely serve as a core food or sheltering resource. 

We know most about the six species of Fraxinus 

where ash has been identified as being a community 

dominant tree species: black, blue, green, Oregon, 

pumpkin, and white. Among mammals, ungulates 

and lagomorphs (rabbits) are often mentioned as 

feeding on non-woody tissues of ash. Northward, 

green and especially black ash are browse sources 

for moose (Elias, 1987) and the white-tailed deer 

(Odocoileus virginianus Zimmermann). A wide 

range of rodents, but especially chipmunks, mice, 

and squirrels, consume the winged seeds. And, while 

we found little mention of such in the literature, 

undoubtedly North American beavers (Castor 

canadensis Kuhl) consume ash across their range. 

Ash seeds are regarded to be of moderate importance 

to seed-eating, woodland or forest dwelling birds 

such as cardinals, chickadees, finches, and grosbeaks. 

Grouse, quail, and turkey are ground feeders 

known to consume ash seeds (Martin et al., 1951). 

Given the propensity of the genus for wetlands, the 

importance of ash seeds to waterfowl has likely been 

underestimated – we only found specific mention of 

wood ducks (Aix sponsa [L.]) feeding on ash samaras 

(Martin et al., 1951). In forests where Fraxinus 

are dominants, ashes also provide cover (e.g., for 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Table 3. Vertebrates that feed on Fraxinus. 

Ash Tree Mammals Birds Literature Comments Fraxinus albicansFraxinus americana white tail deer, fox squirrels 

wood ducks, quail, turkey, grouse, bobwhite, finches (esp. purple finch), grosbeaks (esp. pine grosbeak), cardinals, other songbirds 

Elias, 1987; Burns and Honkala, 1990

Fraxinus anomalaFraxinus berlandieriana Fraxinus carolinianaFraxinus cuspidata deer Fraxinus dipetalaFraxinus gooddingiiFraxinus greggii deer, rabbits, ground squir­ rels, other rodents many birds Fraxinus nigra white tail deer, moose, small mammals wood ducks, grouse, turkey, song birds Elias, 1987; Burns and Honkala, 1990Fraxinus papillosaFraxinus profunda white tail deer wood ducks, many other birds Elias, 1987; Burns and Honkala, 1990Fraxinus pennsylvanica 

white tail deer, mule deer, moose, rabbits, squirrels, and other rodents 

wood ducks, quail, turkey, cardinals, finches Elias, 1987; Burns and Honkala, 1990 large seed crops 

Fraxinus quadrangulata white tail deer wood ducks, quail, turkey, songbirds Elias, 1987 Fraxinus nigra white tail deer, moose, small mammals wood ducks, grouse, turkey, song birds Elias, 1987; Burns and Honkala, 1990Fraxinus velutina Elias, 1987 “little value to wildlife” Fraxinus spp. chipmunks Martin et al., 1951; Rhoads and Block, 2005 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

13 14 15 

16 17 18 

19 20 

Figures 13 - 20. Ash-specialist insects that represent some of the larger taxa threatened by EAB. (13) Tropidosteptes cardinalis, 

Family Miridae (Photo courtesy Mike Quinn); (14) Leptoypha mutica, Family Tingidae. (Photo courtesy Tom Murray); (15) Philtraea 

elegantaria, Family Geometridae (Photo DLW); (16) Sphinx franckii, Family Sphingidae (Photo DLW); (17) Sphinx kalmiae, Family 

Sphingidae (Photo DLW); (18) Dynastes granti, Family Scarabaeidae (Photo courtesy Margarethe Brummerman); (19) Lignyodes 

helvolus, Family Curculionidae (Photo courtesy Bill Johnson); (20) Xylorctes thestalus, Family Scrarabeidae. (Photo courtesy Richard 

Hayes) 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

32 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

moose [Gould and Bauer, 2009]) and above-ground 

structure important to vertebrate wildlife for roosting 

and nesting. Ash trees with broken tops or otherwise 

damaged stems sometimes form cavities which are 

used by a variety of birds, bats, and other animals. 

One ash community type warrants special 

mention, i.e., woodland pools dominated by pumpkin 

ash (F. profunda) (Figs. 7, 9). In southeastern Michigan, 

portions of Ohio, and presumably elsewhere, pumpkin 

ash is sometimes the sole or dominant tree that 

grows in the standing water of vernal and permanent 

(fishless) forest pools and as such provides all or much 

of the canopy closure. Ash-dominated woodland and 

forest pools are an important breeding habitat for 

five species of mole salamanders in the Midwestern 

United States (spotted [Ambystoma maculatum Shaw], 

Jefferson [A. jeffersonianum (Green)], blue-spotted 

[A. laterale Hallowell], small-mouthed [A. texanum 

Matthes], and marbled [A. opacum Gravenhorst]), 

and an occasional breeding habitat for the eastern 

tiger salamander (A. tigrinum Green). Many of these 

salamanders are important conservation targets 

that receive legal protection. Of these, the marbled 

salamander may be the most vulnerable because 

females lay their eggs in mud during the fall, in 

anticipation of autumn and winter rains (Degraaf and 

Rudis, 1986; Pfingsten et al., 2013; Kenney, 1995). 

Greater sun exposure due to canopy loss could affect 

the hydrology of wetlands, especially in the fall, 

before rains and snow melt have had a chance to fill 

them. Most worrisome is that, in Ohio, pumpkin ash 

is sometimes the only tree found growing in these 

saturated to flooded soils where mole salamanders and 

other wildlife breed (Jim McCormac, pers. comm.). 

While much wildlife will experience detrimental 

effects from ash elimination, no doubt some 

vertebrates will benefit. Where EAB has invaded in 

the Midwestern United States, woodpecker numbers 

have spiked in the vicinity of infestations because 

EAB larvae serve as an abundant, easily harvested 

food resource and dying ash provide nesting trees 

for the birds (Cappaert et al., 2005b; Koenig et 

al., 2013). Similarly, standing dead ash trees are 

preferred roosting and nesting sites for many other 

vertebrates and will, for a limited time, benefit wildlife 

posthumously. Canopy gaps left by these dying ash 

species may also allow fruit-producing shrubs such 

as Cornus, Lonicera, and Rhamnus (two of which are, 

unfortunately, non-native invasives) to colonize and 

thrive, the fruits of which will benefit a variety of fruiteating birds and mammals. 

EFFECTS ON ASH-FEEDING
 

INVERTEBRATES
 

We identify 98 Fraxinus-dependent invertebrate herbivores (or inquilines) as potentially threatened by the 

spread of EAB, 45 of which are reported here for the first 

time (Figs. 13-20). Because our compilation of Fraxinus 

feeders was a bottom-up tabulation for all insects and 

mites, built upon the collective knowledge of more than 

80 taxonomic experts, we feel the data in Table 4 offer 

a unique look at the taxonomic distribution of ash-specialist herbivores from the estimated 70,000 species 

of North American insects (Arnett, 2000) and Acari 

(mites). Specialist herbivores that would be imperiled or 

extirpated in the United States and Canada by the loss 

of Fraxinus include mites (n = 6) and members of five 

insect orders: Lepidoptera (n = 32), Hemiptera (n = 25), 

Coleoptera (n = 24), Diptera (n = 9), and Hymenoptera 

(n = 3) (Fig. 21). The most speciose lineage of metazoans 

on the planet, beetles, had fewer specialists than Lepidoptera and essentially equivalent richness to that of Hemiptera. While the focal taxon of our study was Fraxinus 

and related Oleaceae, we suspect that the proportions 

represented here are likely to apply across most temperate woody, broadleaf plant taxa, and may well apply to 

other continental biogeographic provinces as well. 

Four genera contain six or more species that will be 

threatened by the spread of EAB; in decreasing diversity 

these include Tropidosteptes plant bugs (Miridae) (n = 

14) (Fig. 13), Hylesinus bark beetles (Curculionidae) (n = 

7), Lignyodes seed weevils (Curculionidae) (n = 7) (Fig. 

19), and Sphinx hawkmoths (n = 6) (Sphingidae) (Figs. 

16, 17). Four other genera contain noteworthy radiations 

on Fraxinus: Dasineura gall midges (Cecidomyiidae), 

Prociphilus aphids (Aphididae), Philtraea inchworms 

(Geometridae) (Fig. 15), and Sympistis sallows 

(Noctuidae). 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

33 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

 

Figure 21. At risk arthropod herbivores by taxon and imperilment score. 

Charismatic Arthropod Herbivores 

The sphingids or hawkmoths deserve special mention 

because of their beauty, size, and popularity (with 

moth watchers, photographers, and collectors), 

as well as their vulnerability and importance in 

vertebrate diets. Furthermore, the degree of sphingid 

imperilment has heretofore been underestimated. 

Gandhi and Herms (2010) listed eight native and one 

exotic species of sphingids as potentially affected by 

EAB invasion; the only sphingid that they ranked as 

highly to moderately imperiled by EAB was Manduca 

brontes, a Caribbean and South Florida species that 

feeds on Tecoma stans (L.) Juss. ex Kunth in the 

Bignoniaceae. Fraxinus host records for the moth 

were determined to be erroneous by Robinson et al. 

(2002); we exclude this species from our assessment. 

Six sphingids that were regarded as generalists3

 of 

3 Sphinx canadensis, S. chersis, S. kalmiae, and S. franckii, Manduca jasminearum, and Ceratomia undulosa could be classified 

 low or moderate endangerment risk

 in their compilation are treated here as imperiled 

ash specialists: Ceratomia undulosa, Manduca 

jasminearum, Sphinx canadensis, S. chersis, S. franckii 

(Fig. 16), and S. kalmiae (Fig. 17). We add three 

resident hawkmoths not mentioned 

in previous ecological assessments of the North 

American sphingid fauna: Ceratomia sonorensis, 

Sphinx libocedrus, and S. near chersis. We assign 

endangerment risks to these nine ash-dependent 

as polyphagous taxa if one consults treatments such as Covell 

(2005), Wagner (2005), Tuttle (2007), Robinson et al. (2014), etc. 

But if records >50-years old or exceptional reports are excluded, 

all are better regarded as imperiled Fraxinus or Oleaceae 

specialists. Older literature is fraught with misidentifications 

and erroneous host records: For example, the host records of 

Ulmus for S. franckii and M. jasminearum are almost certainly 

based on misidentifications of larval Ceratomia amyntor (Geyer, 

1835), an elm feeder. To the best of our knowledge (and that of 

Jim Tuttle in litt.) none of these six species has been collected 

on host plants outside of the Oleaceae in our lifetimes, and all 

but S. kalmiae (which can be found on other Oleaceae) are best 

considered Fraxinus specialists. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

34 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Table 4. Specialist herbivores on Fraxinus and related Oleaceae.

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Acari Eriophyidae Aceria fraxinifl ora (Felt) Fraxinus americana, F. latifolia High flower gall Felt, 1918; Baker et al., 1996; Ron Och­ ua pers. comm. Acari Eriophyidae Aceria fraxini (Garman) 

Fraxinus americana, F. latifolia, F. pennsylvanica 

High leaf gall Felt, 1918; Baker et al., 1996 

Acari Eriophyidae Tegolophus califraxini (Keifer) Fraxinus dipetala, F. velutina High leaves Jeppson et al., 1975; Baker et al., 1996 Acari Tenuipalpidae Brevipalpus fraxini DeLeon Fraxinus, F. profunda High leaves 

DeLeon, 1961; Baker and Suigong, 1988; Ron Ochua pers. comm. 

Acari Tenuipalpidae Brevipalpus cardinalis (Banks) Fraxinus velutina, F. albicans High unknown Banks, 1915; Baker and Suigong, 1988; Johnson, 2007 Coleoptera Buprestidae Agrilus subcinctus Gory Fraxinus pennsylvanica, Ligustrum High to Moderate cambium 

Bright, 1987; Ted MacRae unpubl. data; Richard Westcott in litt. 

Coleoptera Buprestidae Trigonogya reticulaticollis (Schaeff er) Fraxinus berlandieriana High? recently dead wood 

MacRae, 2006; Ted MacRae unpubl. data; Richard Westcott in litt. 

Confirmed larval host; Knull (1937) recorded adults collected on F. caroliniana, but that is a misidentification of F. berlandieriana (Richard 

Westcott in litt.). Host range needs more study. 

Coleoptera Chrysomelidae Capraita sexmaculata (Illiger) 

Chionanthus virginicus, Fraxinus americana, F. berlandieriana,Forestiera ligustrina 

High to Moderate leaves 

Clark et al., 2004; Shawn Clark in litt.; Ed Riley in litt. 

Probably obligatory on ash; adult diet includes other Oleaceae hosts. 

Coleoptera Chrysomelidae Trichaltica tibialis (Jacoby) Fraxinus High root Clark et al., 2004; Shawn Clark in litt.; Ed Riley in litt. Larvae root feeders; almost certainly spe­ cialists. 

Coleoptera Chrysomelidae Trichaltica scabricula (Crotch) Fraxinus High root Clark et al., 2004; Shawn Clark in litt. Larvae root feeders; almost certainly spe­ cialists. 

Coleoptera Curculionidae Hylesinus aculeatus (Say) Fraxinus americana, F. pennsylvanica High cambium 

Blatchley and Leng, 1916; Wood, 1982; Atkinson, 2014, Anthony Cognato in litt. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

35 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Coleoptera Curculionidae Hylesinus californicus (Swaine) 

Fraxinus americana, F. latifolia, F. pennsylvanica, F. velutina, Olea europaea 

High to Moderate cambium 

Wood, 1982; Langor and Hergert, 1993; Atkinson, 2014; Anthony Cognato in litt. 

Coleoptera Curculionidae Hylesinus criddlei

(Swaine) 

Fraxinus americana, F. pennsylvanica High cambium 

Atkinson, 2014; Anthony Cognato in litt. 

Coleoptera Curculionidae Hylesinus fasciatus LeConte Fraxinus americana High cambium 

Blatchley and Leng, 1916; Wood, 1982; Atkinson, 2014; Anthony Cognato in litt. 

Coleoptera Curculionidae Hylesinus mexicanus (Wood) Fraxinus albicans, Forestiera, Ligustrum, Olea Moderate cambium Atkinson, 2014; Anthony Cognato in litt. Coleoptera Curculionidae Hylesinus oregonus (Blackman) Fraxinus latifolia High cambium 

Wood, 1982; Burns and Honkala, 1990; Atkinson, 2014; Anthony Cognato in litt. 

Coleoptera Curculionidae Hylesinus pruinosus Eichhoff Fraxinus americana High cambium Wood, 1982; Atkin­ son, 2014; Anthony Cognato in litt. Coleoptera Curculionidae Lignyodes arizonicus (Sleeper) Fraxinus velutina High seed Clark, 1980; Robert Anderson pers. comm. Coleoptera Curculionidae 

Lignyodes auratus Clark 

Fraxinus latifolia High seed 

Clark, 1980; Robert Anderson pers. comm. 

Coleoptera Curculionidae Lignyodes bischoffi (Blatchley) 

Fraxinus americana, F. nigra, F. pennsylvanica, Syringa 

High to Moderate seed 

Knull, 1932; Clark, 1980; Robert Anderson pers. comm. 

Coleoptera Curculionidae Lignyodes fraxini 

(LeConte) Fraxinus americana High seed 

Clark, 1980; Robert Anderson pers. comm. 

Coleoptera Curculionidae Lignyodes helvolus (LeConte) Fraxinus americana, F. berlandieriana, F. nigra, Syringa High to Moderate seed Clark, 1980; Robert Anderson pers. comm. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

36 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Coleoptera Curculionidae Lignyodes helvolus (Le- Conte) Fraxinus americana, F. berlandieriana, F. nigra, Syringa High to Moderate seed Clark, 1980; Robert Anderson pers. comm. 

Coleoptera Curculionidae Lignyodes horridulus (Casey) Fraxinus latifolia, F. pennsylvanica , F. velutina, Syringa High to Moderate seed Clark, 1980; Robert Anderson pers. comm. Coleoptera Curculionidae 

Lignyodes ocularis(Casey) Fraxinus High seed 

Clark, 1980; Robert Anderson pers. comm. 

Coleoptera Curculionidae Psomus armatus (Dietz) (including politus) Fraxinus americana High seed 

Blatchley and Leng, 1916; Arnett et al., 2002; Charles O’Brien in litt.; Richard Westcott in litt. 

Coleoptera Scarabaeidae Dynastes granti Horn Fraxinus velutina High-see com­ ments new shoot feeder 

Bill Warner in litt.; Pat Sullivan pers. comm.; Margarethe Brummerman pers. comm. 

Larvae may be generalists but adults feed on ash; beetle rare or absent away from Fraxinus (Bill Warner in litt.). 

Coleoptera Scarabaeidae Dynastes tityus L. Fraxinus High-see com­ ments new shoot feeder Glaser, 1976 Adults feed (and mate?) at wounds gnawed into ash shoots. 

Coleoptera Scarabaeidae Xyloryctes jamaicensis (Drury) Fraxinus americana High root Ratcliff e, 2009 See discussion in Rat- cliff e 2009. 

Coleoptera Scarabaeidae Xyloryctes thestalus Bates 

Fraxinus velutina and likely other Fraxinus species, esp. in Mexico 

High root Ratcliff e, 2009 See discussion in Rat- cliff e 2009. 

Diptera Agromyzidae Phytobia sp. Fraxinus americana, F. pennsylvanica High cambium Solomon, 1995; Sonja Sheff er in litt. 

Diptera Cecidomyiidae Contarinia thalactri (Felt) (including fraxini) Fraxinus, F. americana High leaf gall (inquiline) Gagné, 1989 Phytophagous inquiline in galls of Dasineura tumidosae. 

Diptera Cecidomyiidae Contarinia n. sp. Fraxinus pennsylvanica High samara gall Gagné, 1989 

Samara exocarp gall; gregarious; undescribed evidently; near European species C. marchali. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

37 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Diptera Cecidomyiidae Contarinia n. sp. Fraxinus pennsylvanica High seed or samara gall Raymond Gagné in prep. 

Seed or samara gall; undescribed; not near European species C. marchali. 

Diptera Cecidomyiidae Dasineura apicata (Felt) Fraxinus americana High leaflet gall Felt, 1918; Gagné, 1989 

Diptera Cecidomyiidae Dasineura fraxinifolia (Felt) Fraxinus americana High leaflet gall Felt, 1918; Gagné, 1989 

Diptera Cecidomyiidae Dasineura pellex (Osten Sacken) Fraxinus americana High leaflet gall Felt, 1918; Gagné, 1989; Raymond Gagné in litt. 

Diptera Cecidomyiidae Dasineura tumidosae (Felt) Fraxinus americana High leaflet gall Gagné, 1989 

Diptera Cecidomyiidae Dasineura n. sp. Fraxinus pennsylvanica High seed gall Raymond Gagné in prep. 

Reared from seed collection from Ontario (Raymond Gagné in prep.). 

Hemiptera Aphididae Prociphilus americanus (Walker) Abies, Fraxinus dipetala, F. latifolia, F. velutina High phloem DeAngelis, 1998; TTD, 2014; Carol von Dohlen in litt. Abies is alternate host. 

Hemiptera Aphididae Prociphilus fraxinifolii (Riley) Fraxinus americana, F. nigra, F. velutina High phloem TTD, 2014; Carol von Dohlen in litt. 

Hemiptera Aphididae Prociphilus pergandei Smith Fraxinus americana High phloem Blackman and Eas­ top, 1994; Carol von Dohlen in litt. Hemiptera Aphididae Prociphilus probosceus (Sanborn) Fraxinus High phloem Blackman and Eas­ top, 1994; Carol von Dohlen in litt. Hemiptera Diaspididae Diaspidiotus fraxini (McKenzie) Fraxinus velutina High phloem Miller et al., 2014a; Douglass Miller in litt. Few Diaspididae are specialists; confirma­ tion of monophagy is needed. 

Hemiptera Diaspididae Diaspis fraxini Ferris Fraxinus velutina var. tourneyi High phloem Miller et al., 2014b; Douglass Miller in litt. 

Type locality about 42 miles from Arizona border. Uncertain if species has been reported from US; few Diaspididae are specialists (Ben Normark pers. comm.); confirmation of monophagy is needed. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

38 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Hemiptera Miridae Bisulcopsallus texanus (Knight) Fraxinus High phloem TTD, 2014; Michael Schwartz in litt. 

Hemiptera Miridae Tropidosteptes adustus (Knight) Fraxinus americana High phloem Henry, 1980; TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes amoenus (Reuter) Fraxinus americana, F. latifolia, F. pennsyl­ vanica High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes brooksi Kelton Fraxinus High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes canadensis Van Duzee Fraxinus, F. pennsyl­ vanica High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes cardinalis Uhler Fraxinus americana High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes glaber (Knight) Fraxinus americana High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes illitus (Van Duzee) Fraxinus velutina High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes neglectus (Knight) Fraxinus pennsylvanica High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes pacificus (Van Duzee) Fraxinus latifolia, F. velutina High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes pettiti Reuter Fraxinus High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes populi (Knight) Fraxinus americana, F. pennsylvanica High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes rufi venosus (Knight) Fraxinus High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Miridae Tropidosteptes tricolor Van Duzee Fraxinus pennsylvanica High phloem TTD, 2014; Michael Schwartz in litt. 

Hemiptera Miridae Tropidosteptes vittiscu­ tis (Knight) Fraxinus americana High phloem TTD, 2014; Michael Schwartz in litt. Hemiptera Pentatomidae Banasa rolstoni Th omas & Yonke Fraxinus velutina High phloem Donald Th omas pers. comm. More study needed; oth­ er Banasa sp. are known to be generalists. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

39 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Hemiptera Tingidae Leptoypha costata Parshley Chionanthus, Fraxinus High to Moderate phloem 

Usinger, 1945; Drake and Ruhoff , 1965; Tom Henry in litt; Chionanthusrecord from Laura Miller in litt. 

Carya ovata, Corylus,

and Hamamelis recordsfor this species likely in error (Tom Henry in litt.). 

Hemiptera Tingidae Leptoypha minor McAtee (including nubilis) Fraxinus latifolia, F. velutina, and other Oleaceae High to Moderate phloem Usinger, 1945; Drake and Ruhoff , 1965; Tom Henry in litt. Ceanothus, Populus and other non-Oleaceae hosts in error (Tom Henry in litt.). 

Hemiptera Tingidae Leptoypha mutica (Say) Chionanthus, Fraxinus americana High to Moderate phloem 

Froeschner, 1944; Usinger, 1945; Drake and Ruhoff , 1965; Tom Henry in litt.; Laura Miller in litt 

Forestiera records likely refer to another species (Tom Henry in litt.). 

Hymenoptera Tenthredinidae Eupareophora parca (Cresson) Fraxinus americana, F. nigra, F. latifolia, F. pennsylvanica High new leaves Williams, 2007; David Smith in litt. Pecan record is doubtful (David Smith in litt.). 

Hymenoptera Tenthredinidae Tethida barda (Say) Fraxinus americana High new leaves David Smith in litt. 

Hymenoptera Tenthredinidae Tomostethus multicinctus (Rohwer) Fraxinus americana, F. latifolia High new leaves Langford and McConnell, 1935; David Smith in litt. Lepidoptera Apatelodidae Olceclostera angelica (Grote) Fraxinus, Syringa High to Moderate mature leaves Wagner, 2005, 2007; Robinson et al., 2014 

Lepidoptera Geometridae Hydrelia near inornata Fraxinus americana High mature leaves Wagner et al., 2002 

Validity of this taxon in need of (molecular) verification. 

Lepidoptera Geometridae Philtraea elegantaria (Hy. Edwards) Fraxinus gooddingii High leaves DLW unpubl. data Lepidoptera Geometridae Philtraea latifoliae Buckett Fraxinus latifolia Very High leaves Buckett, 1970; Wag­ ner, 2007 

Only known from a few counties in Central California and evidently declining. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

40 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Lepidoptera Geometridae 

Philtraea paucimacula Barnes and McDunnough Fraxinus greggii and Lycium Moderate but see comments leaves Noel McFarland pers. comm.; Wag­ ner unpubl. data 

F. greggii record fromLaredo, TX (Noel McFarland pers. comm.) and Big Bend by DLW; Lycium in Big Bend NP from Wagner unpubl. data but possibly two taxa involved in which case the ash feeder is imperiled . 

Lepidoptera Geometridae Philtraea surcaliforniae Buckett Fraxinus dipetala High leaves Buckett, 1970; Wag­ ner, 2007 Lepidoptera Geometridae Plagodis kuetzingi (Grote) Fraxinus americana, F. quadrangulata High leaves Wagner, 2007 Lepidoptera Gracillariidae Caloptilia fraxinella (Ely) Fraxinus americana, F. nigra, F. pennsylvanica High new leaves Johnson and Lyon, 1988; Pohl et al., 2004; Wagner, 2007 

Ligustrum as a host is listed in error in previous tabulations; that record traces to C. cucullipennella (Charley Eiseman in litt.). 

Lepidoptera Gracillariidae Caloptilia n. sp. Fraxinus latifolia High new leaves Wagner, 2007, unpubl. data Found along creeks in central and northern California. 

Lepidoptera Gracillariidae Marmara basidendroca Fitzgerald Fraxinus pennsylvanica Very High bark miner that tunnels into root crown Fitzgerald, 1973; Wagner, 2007 Currently known only from Upstate New York. Feeds on single cell layer in cork cambium. 

Lepidoptera Gracillariidae Marmara corticola Fitz­ gerald Fraxinus pennsylvanica Very High green bark miners Fitzgerald, 1973; Wagner, 2007 

Currently known only from Upstate New York. Feeds on single cell layer in cork cambium initially and then tunnels into deeper cork layers. 

Lepidoptera Gracillariidae Marmara fraxinicola Braun Fraxinus americana, F. pennsylvanica High green bark miners 

Fitzgerald and Simeone, 1971; Fitzgerald, 1973; Wagner, 2007 

Feeds on single cell layer in cork cambium. 

Lepidoptera Noctuidae Chloronycta tybo (Barnes) Fraxinus velutina High mature leaves Schmidt et al., 2014 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

41 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Lepidoptera Noctuidae Copivaleria grotei Mor­ rison Fraxinus americana High new leaves Wagner, 2007; Rob­ inson et al., 2014 

Lepidoptera Noctuidae Papaipema furcata (J. B. Smith) Fraxinus americana, F. nigra, F. pennsylvanica High new shoot feeder (borer) Wagner, 2007; Rob­ inson et al., 2014 

Non-Fraxinus hosts are 

insignificant, incidental, or erroneous (Eric Quinter in litt.). Larvae feed only in vigorous growing shoots usually of saplings. 

Lepidoptera Noctuidae Sympistis chionanthi (J. E. Smith) Chionanthus virginicus, Fraxinus americana, F. nigra, F. pennsylvanica High to Moderate new leaves Wagner, 2007; Wagner et al., 2011; Robinson et al., 2014 Triosteum records likely in error and refer to S. forbesi (Zacharczenko et al. 2014). 

Lepidoptera Noctuidae Sympistis fortis (Grote) Fraxinus, F. latifolia High new leaves 

Robinson et al., 2014; CDFA card fi le pest database 

CDFA record for Keckiella antirrhinoides as a host likely derives from a misidentification of S. picina 

Lepidoptera Noctuidae Sympistis punctilinea (Hampson) Fraxinus, F. velutina High new leaves Crumb, 1956; CDFA card fi le pest database Lepidoptera Noctuidae Sympistis heterogena (A. Blanchard) Fraxinus cuspidata High new leaves DLW unpubl. data 

New leaves of F. greggiigrowing in Chisos Basin, Big Bend NP. Spring active. 

Lepidoptera Pyralidae Palpita magniferalis (Walker) Fraxinus americana, F. nigra, F. pennsylvanica High leaves Robinson et al., 2014 Lepidoptera Sesiidae Podosesia aureocincta Purrington & Nielson Fraxinus, F. americana, F. pennsylvanica, Olea High to Moderate xylem 

Eichlin and Duckworth, 1988; Wagner, 2007; Robinson et al., 2014 

Sister to syringae: slight flight period and genitalic diff erences; COI barcode shared with syringae; reports from Olea should be verified. 

Lepidoptera Sphingidae Ceratomia sonorensis Hodges Fraxinus velutina High mature leaves Tuttle, 2007; Wagner, 2005, 2007 Lepidoptera Sphingidae Ceratomia undulosa (Walker) 

Chionanthus virginicus, Fraxinus american, F. caroliniana, F. nigra, 

F. pennsylvanica, Ligustrum, and Syringa 

High to Moderate mature leaves Tuttle, 2007; Wagner, 2005, 2007 

DLW discounts all records other than those on Oleaceae: Fraxinuspreferred host. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

42 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Lepidoptera Sphingidae Manduca jasminearum (Guérin) Fraxinus, Syringa High mature leaves Tuttle, 2007; Wagner, 2005, 2007 DLW discounts all records other than those on Oleaceae. 

Lepidoptera Sphingidae Sphinx canadensis Boisduval 

Fraxinus americana (origin of this host requires verification) F. nigra (preferred host) 

Very High mature leaves Tuttle, 2007; Wagner, 2005, 2007 

DLW discounts all records other than those on Oleaceae. another Fraxinus species likely to be principal host species south of Ohio River. 

Lepidoptera Sphingidae Sphinx chersis (Hübner) 

Fraxinus americana, F. pennsylvanica, F. velutina, Ligustrum, Syringa, other Oleaceae 

High to Moderate mature leaves Tuttle, 2007; Wagner, 2005, 2007 DLW discounts all records other than those on Oleaceae. 

Lepidoptera Sphingidae Sphinx near chersis Fraxinus velutina High mature leaves Chris Schmidt in litt. 

DNA barcodes suggestive that Arizona populations of S. chersisrepresent n. sp. sister to S. mexicana (Chris Schmidt in litt.) 

Lepidoptera Sphingidae Sphinx franckii Neumoegen Fraxinus americana, Ligustrum Very High mature leaves Tuttle, 2007; Wagner, 2005, 2007 

DLW discounts all records other than those on Oleaceae; already uncommon and declining; Fraxinus preferred host. 

Lepidoptera Sphingidae Sphinx kalmiae J. E. 

Chionanthus virginicus, Fraxinus ameicana, F. nigra, F. pennsylvanica, Ligustrum, Syringa 

High to Moderate mature leaves Tuttle, 2007; Wagner, 2005, 2007 DLW discounts all records other than those on Oleaceae. 

Lepidoptera Sphingidae Sphinx libocedrus 

Forestiera spp., Fraxinus gooddingii, F.greggii 

Moderate mature leaves Tuttle, 2007 Forestiera likely the principal host. 

Lepidoptera Yponomeutidae Zelleria near hepariella Fraxinus latifolia High leaves Wagner, 2007 

Report by Wagner (2007) as Z. hepariellain error; the use of hepariella traces to preliminary determination 

by Tom Eichlen (in litt.); taxonomy still under study. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

43 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Table 4. (continued) 

Taxon Family Scientifi c Name Confirmed Hosts Risk Rating Guild Reference(s) Comments 

Lepidoptera Yponomeutidae Zelleria near semitincta Fraxinus dipetala High? leaves John DeBenedictis unpubl. data 

A similar appearing moth occurs in southern California on Forestiera. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

44 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Figure 22. Mating pair of North America’s largest beetle, Dynastes granti (Photo courtesy 

Margarethe Brummerman). So far as known, actively growing ash shoots are the principal feeding 

site for this behemoth, which sometimes exceeds 80 mm in length. Males chew a lesion into new 

growth and females are paired as they arrive at the wound. Curiously, its more widespread cousin, 

the Eastern Hercules beetle; Dynastes tityus, is virtually unstudied as an adult. The only adult 

feeding record of which we are aware, again is for a Fraxinus (Glaser 1976). Grant’s rhinoceros 

beetle is quite sought-after by photographers and collectors; persons (even families) with 

interests in Coleoptera, sometimes travel from as far away as Japan and Korea to see the beetle. 

See also caption for Figure 23. 

species as Very High (n = 2), High (n = 3), High 

to Moderate (n = 3), and Moderate (n = 1). Three 

of the nine have restricted global distributions and 

are ranked as G4 species in NatureServe Explorer 

(2014): Manduca jasminearum, Sphinx canadensis, 

and S. franckii (Fig. 16). The first of these is already 

in decline along the northern portion of its range 

(NatureServe Explorer, 2014), and sphingids (and 

especially members of the nominate genus Sphinx) 

have been identified as a group in decline across 

much of the northeastern United States, perhaps 

due to the exotic tachinid Compsilura concinnata 

(Meigen) (Wagner, 2012) or an as yet unidentified egg 

parasitoid (Sam Jaffe, unpublished data). 

One of the most surprising findings from our 

study is that one of North America’s largest, and 

attention-worthy insects may be threatened by EAB: 

the western rhinoceros beetle (Dynastes granti), 

whose adults occasionally exceed 80 mm in length 

(Figs. 18, 22). While this large scarab is a generalist 

as a larva, feeding in dead wood of various tree 

species, its adult may prove to be a specialist that 

feeds primarily on the new growth of velvet ash 

in Arizona. Courting males chew into the cambial 

layers of an ash tree and then await the arrival of 

females (which presumably feed and mate at the 

wound site). The best known and most reliable 

locations for the beetle occur in the vicinity of velvet 

ash, where the adults have access to vigorously 

growing green shoots (Margarethe Brummerman, 

Patrick Sullivan, and Bill Warner, all in litt.). Beetle 

collectors visit the southwestern United States with 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

the Grant’s rhinoceros beetle as a common focus of 

their itineraries. Rhinoceros beetles are also popular 

pets in some Asian countries; we know of instances 

of Asian families traveling to Arizona primarily to 

acquire living Dynastes adults to keep as pets and 

captive breeding (Fig. 23). Dynastes granti is even 

occasionally sold in Japanese pet shops and has 

appeared in staged beetle fights. 

Less is known about the habits and dietary 

proclivities of the eastern rhinoceros beetle (Dynastes 

tityus), but it too is known to chew into shoots of ash 

and feed at the wounds (Glaser, 1976); no other adult 

food plants are known to us. Ratcliffe (2009) called 

attention to the threat of EAB to two other rhinoceros 

beetles in the genus Xyloryctes, which reach lengths 

close to 30 mm (Fig. 20). Both North American 

species are specialists on ash roots as larvae. If even a 

few of the species mentioned above were to disappear, 

the losses to North American arthropod fauna would 

be great (in both senses of the word). 

Figure 23. Entomophily. The insect zoo at the United States 

Museum of Natural History, ranks only behind dinosaurs 

as a public draw. Insects also enjoy considerable favorable 

attention in many Asian countries. This photo is from an insect 

exhibition held in the Tokyo Tower over a six-week span in 2013 

(http:www.japantrends.com/tokyo-tower-insect-exhibition/) 

(Photo courtesy of Tokyo Tower, Nippon Television City 

Corporation). More than 16,000 insects were on display, many 

of which were alive in the featured insect jungle. The scene 

above shows a beetle enclosure with many horned scarabs, 

kindred to and perhaps even including the North American 

Dynastes and Xyloryctes that are listed in Table 4 and shown in 

Figures 18, 20, and 22. Asian families are also known to travel 

annually to the Southwest United States to look for live D. 

granti adults to be kept as family pets and bred. 

Figure 24. Feeding guilds of specialist herbivores on ash. Chart shows 98 species of ash 

specialists divided by feeding guild: bark (3), phloem (26), cambium (9), xylem (2), root (4), 

seed (8), new shoot feeder (3), gall-former (10), leaf miner (2), leaves (32), and unknown (1). 

Some species could be included into two feeding guilds, e.g., gall formers may form galls on 

seeds or leaves, etc. In these cases, we grouped individuals into the most applicable guild. See 

Table 4 for additional notes on feeding guilds. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Feeding Guilds and Specificity of Arthropod 

Herbivores 

We group the 98 phytophagous arthropods identified 

in Table 4 into ten feeding guilds (Fig. 24). The degree 

of host specificity for the majority of the species listed 

in Table 1 is not known in detail. We are unaware of any 

taxonomically comprehensive study of ash herbivores 

where researchers thoroughly sampled across the 

spectrum of available Fraxinus (and other Oleaceae). It 

is our belief that most Fraxinus specialists (as defined in 

this work) consume a spectrum of available ash species 

growing in a given locale. Stated differently, we see little 

indication that the phylogenetic, physiological, and 

morphological differences across the genus Fraxinus 

are so great that ash-specialized herbivores are routinely 

restricted to a single species or even Section of the 

genus (contrary to what one might be led to believe 

from published host records). In the western United 

States many of the herbivores listed in Table 4 are 

associated with a single ash species simply because only 

one Fraxinus (or member of the Oleaceae) occurs at a 

given locale. In eastern North America, in cases where 

only Fraxinus (without a species indicated) is listed 

in Table 4, the host is likely assignable to F. americana 

and/or F. pennsylvanica. Based on our literature review, 

communications with >80 taxonomists, and DLW’s 30­

year rearing program of North American Lepidoptera 

(that has encompassed more than 2,000 species 

representing more than 50 families, including miners, 

gall-formers, wood feeders, and others), the following 

generalities emerged. 

Wood feeders. As reflected in our results, wood 

feeders (restricted here to taxa consuming mostly 

subcambial tissues including dead and live wood 

feeders) are seldom specialized in diet, e.g., not one 

of North America’s 1000 cerambycids is known to be 

a Fraxinus specialist as a larva. We list only two wood 

feeders: the buprestid, Trigonogya reticulaticollis, 

whose host range is not well investigated and the 

clearwing borer Podosesia aureocincta, which is likely 

oligophagous on Oleaceae. 

Phloem feeders. We identify 25 Fraxinus 

specialist, phloem-feeding hemipterans. While several 

of these appear to be monophagous, we believe that 

this is a sampling artifact and that the species in Table 

Figure 25. Marmara fraxinella, Family Gracillariidae (Photo 

courtesy Charley Eiseman). Leafminers of the genus Marmara 

are specialized herbivores. Three North American Marmara 

are known only to feed on Fraxinus, and two of these mine 

only in the bark of young, actively growing ash trees. 

Figure 26. Four males of the two-tailed swallowtail (Papilio 

multicaudata), Arizona’s state butterfly, puddling in Oak Creek 

canyon, outside of Sedona, Arizona. Larvae feed on members 

of three plant families, but only ashes are present in some of 

the western canyons where this large swallowtail butterfly 

occurs. (Photo courtesy Tyger Gilbert, www.TygerGilbert.com) 

4 will be found to feed on multiple species of ash. The 

aphids (n = 3), diaspidid scales (n = 2), and mirids 

(n = 15) appear to be obligate Fraxinus feeders. Tom 

Henry (in litt.) believes that the three tingids listed 

in Table 4 are oligophagous on Oleaceae and that 

contrary host records are unreliable. The diet breadth 

of the pentatomid B. rolstoni requires further study 

as very few stink bugs are known to be host plant 

specialists. 

Cambium feeders. We record seven bark beetles 

and a cambium-mining agromyzid (Phytobia sp.) as 

ash specialists. The only buprestid identified as an 

ash specialist – from a family with more than 760 

North American species – was Agrilus subcinctus, a 

cambium miner (of course, we exclude A. planipennis). 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

As a subcategory to cambium feeders, we include the 

three gracillariids that mine in green bark. Marmara 

basidendroca tunnels into cambial layers at least for 

part of its life cycle (Fitzgerald, 1973). This gracillariid 

and two of its congeners, M. corticola and M. 

fraxinicola are all highly specialized insects regarded to 

be at high risk (Fig. 25). 

New shoot feeders. We include the borer 

Papaipema furcata (Noctuidae), which so far as is 

known, tunnels only in new growth of Melioides 

Fraxinus. Both western and eastern rhinoceros 

beetles (D. granti and D. tityus) can be provisionally 

placed here because adults are only known to feed at 

vigorously growing shoots of ash. 

Root borers. We report four coleopterans whose 

larvae are ash root specialists – two leaf beetles: 

Trichaltica tibialis and T. scabricula and two scarab 

beetles: Xyloryctes jamaicensis and X. thestalus (Fig. 

20). The extent to which the larvae of these beetles 

accept different species of ash has not been studied, 

although their ranges are broad enough to suggest that 

none is monophagous. 

Seed feeders. Members of this guild, or at least 

the weevils of the genus Lignyodes (Fig. 19), appear to 

be oligophagous. Psomus armatus, so far known only 

from white ash, is expected to feed on other ashes 

based on what is known of the diet breadth of related 

weevils. 

Gall formers. Gall insects are widely recognized to 

be among the most specialized insect herbivores (Felt, 

1918, Gagné, 1989). The two gall-forming eriophyid 

mites that we list have been reported from more than 

one species of Section Melioides ashes. Gagné (in litt.) 

believes that all the cecidomyiid gall formers in Table 1 

will be found to occur on more than one species within 

a Fraxinus Section, but that significant differences are 

likely to exist among Sections. 

Leafminers. There are only two leafminers in 

our study, both members of the genus Caloptilia 

(Gracillariidae). One leafminer, Caloptilia n. sp., is 

an ecological specialist on F. latifolia; its eastern sister 

taxon, C. fraxinella, feeds on at least three species 

from two Fraxinus sections. 

External (chewing) leaf feeders. Only one 

externally feeding lepidopteran is recorded as 

monophagous: Philtraea latifoliae (Geometridae), and 

its dependency on Oregon ash is likely a geographical 

artifact because its host is the only member of the 

Oleaceae that grows where the moth occurs. One 

surprising outcome of our compilation is how 

proportionately few specialist external leaf feeders 

were detected (<32% of the 98 Fraxinus-dependent 

herbivores), though this guild comprises most of the 

insect biomass using ash and the most conspicuous 

herbivores on Fraxinus. Clearly, the insects that live 

and feed inside seeds, stems, or leaves dominate our 

list of species threatened by EAB. 

Oligophages, Polyphages, and Other Trophic 

Levels 

Our ecological assessment focused on specialists; it 

ignored oligophages and polyphages that might be 

affected by ash decline. However, over the course 

of preparing this manuscript, we discovered a few 

instances where an oligophage not treated in our list 

might be affected by EAB. For example, the two-tailed 

swallowtail (Papilio multicaudatus) (Fig. 26) uses 

Fraxinus, Prunus, and Ptelea as hosts in arid lands 

of western North America, but only ash species are 

available in some canyons where this butterfly lives. 

Octotoma (hispine chrysomelids), e.g., O. plicatula 

and O. marginicollis, were not included because their 

leafmining larval stages are specialists on non-ash 

species, even though the adult beetles are believed to 

do much of their adult feeding on Fraxinus species 

(Shawn Clark, in litt.). 

We did not find mention of any specialist 

parasitoids, predators, or pathogens that we could 

confidently state were dependent on an ash herbivore. 

The recently described Mymaromella pala Huber 

& Gibson (Mymarommatidae) is known only from 

ash log collections, but its presumed host is a barkresiding psocid (Huber et al., 2008) likely to dwell on 

other trees as well. Gagné (1989) regards Contarinia 

thalactri to be a phytophagous inquiline in the galls of 

Dasineura tumidosae. However, beyond this inquiline 

record, we did not find mention of any other 

indirectly ash-specialized insects. 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

disCUssion 

Imperilment Risk Ratings 

It is our estimate that no less than 98 species of 

invertebrate herbivores would be appreciably affected 

by an elimination or massive reduction in abundance 

of North America’s 16 native Fraxinus. For these 

herbivores we estimate endangerment risks as Very 

High (n = 5), High (n = 75), High to Moderate (n = 

15), and Moderate (n = 3) (Fig. 21). Forty-five of the 

species-level taxa listed in Table 4 are identified as 

“at risk” for the first time. Eighteen (6%) of the taxa 

identified by Gandhi and Herms (2010) had their 

imperilment status upgraded; twenty six (35%) of 

the species listed in their treatment as being of high 

to moderate endangerment risk are dropped from 

consideration (Appendix 3). A key message deriving 

from this expert-based approach is that researchers 

should use caution when gleaning host records from 

dated literature, the internet, and especially secondary 

and tertiary resources. We found records (and 

especially older host records) to be rife with invalid 

taxa, erroneous identifications, instances where a 

presumed ash specialist was not phytophagous, cases 

where presumed ash specialists were generalists (type 

I errors), cases where presumed oligophagous or 

generalist herbivores were in fact specialists (type II 

errors), and cases where exotic or extralimital taxa 

were included. 

As noted previously, we discounted the ecological 

importance of introduced (exotic) plants, e.g., lilac, 

privet, and olive, as alternative hosts that could 

support sufficiently large populations to ensure a 

taxon’s long-term survival in North America. This 

seems to be a defensible position if one were to invoke 

the precautionary principle in assessing risk. But, we 

also recognize that it is possible that some invasive 

plants (such as Ligustrum) could play a role in the 

survival of some native Oleaceae specialists were EAB 

to eliminate much of the Fraxinus in a region. 

The Very High risk rating – given to just five 

lepidopterans – was reserved for ash specialists 

believed to be at risk or in decline due to other 

causes. Marmara basidendroca and M. corticola 

(both Gracillariidae) are both specialized stem 

miners known only from a restricted area in Upstate 

New York. Philtraea latifoliae (Geometridae) feeds 

exclusively on Fraxinus latifolia and is known only 

from a few counties in central California (Buckett, 

1970). Sphinx canadensis’ rating was raised to Very 

High because it is principally associated with F. nigra, 

an ash that is highly susceptible to EAB infestation 

(Leah Bauer pers. comm.) and which is predicted to 

be increasingly at risk due to climate change (Liang 

and Fei, 2014). Sphinx franckii is already uncommon 

and northern populations are in decline (Wagner, 

2012). 

For perspective on the importance of ash and 

the emerald ash borer, it is useful to compare ash 

decline with what is known about American chestnut 

(Castanea dentata [Marsh.] Borkh.) and its dependent 

herbivore fauna. Opler (1978) listed seven species of 

Lepidoptera that may have gone extinct as a result 

of losing this once ecologically dominant forest tree. 

One of these seven moths has since been rediscovered 

(Synanthedon castaneae [Busck]) (Anagnostakis et al., 

1994), and another listed species, Tischeria perplexa 

Braun, may not be a valid species given that other 

Fagaceae-feeding Tischeria from the eastern United 

States are not chestnut specialists (Braun, 1972)4

. 

Thus, five is a better estimate of the number of moth

 species that have been lost from the North American 

fauna5

 due to American chestnut decline. If one 

compares the number of extinct moths restricted to 

chestnut (n = 5) to the at risk ash-feeding Lepidoptera 

listed in Table 4 (n = 32), one is immediately struck by 

the magnitude of the threat posed by the introduction 

and spread of EAB. North America has not faced a 

threat of this magnitude to its native insect herbivore 

biodiversity from an exotic species over the course of 

the last two centurie. We believe that this is because 

4 Three other Tischeria occur on Castanea dentata – one of 

which, T. castaneaeella, is believed to be quite closely related to 

T. perplexa, the purported Castanea dentata specialist. All three 

of the extant Tischeria that fed on chestnut are breeding on 

red oaks. Given the above, it is DLW’s belief that T. perplexa will 

prove to be a taxonomic synonym. 

5 As a caveat, it is worth noting that no one has systematically 

sampled introduced Castanea or related native Castanea, and 

especially Alleghany chinquapin (C. pumila), which co-occurred 

with American chestnut; nor have workers surveyed nut-producing stands of C. dentata in Ohio, Maine, and elsewhere for the 

missing species. 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

Fraxinus represents a phylogenetically and or 

chemically isolated biological island that is too far 

removed from its allied genera (e.g., Chionanthus, 

Forestiera, exotic Ligustrum, and Oleaeceae) for 

these plants to serve as refuges for Fraxinus specialist 

herbivores over ecological and evolutionary time. 

Data Gaps 

Host ranges for virtually all of the taxa in this study 

remain incompletely known. Targeted herbivore 

surveys of the 16 North American Fraxinus would be 

valuable, especially for understudied ash species and 

those currently under threat from EAB or soon to be 

attacked as the beetle’s range expands. In particular, 

southern ash are poorly studied as they tend to grow 

in swamps and all nine western ash species require 

further research; almost nothing is known of F. 

albicans, F. berlandieriana, F. cuspidata, F. gooddinggii, 

and F. papillosa. Likewise, the importance of other 

native Oleaceae, especially Forestiera, as hosts for ashfeeding herbivores is in need of study. Of critical 

importance to the evaluation of imperilment risk 

is the possibility that other native Oleaceae may 

be susceptible to the emerald ash borer. Only very 

recently did researchers learn that Chionanthus is 

also susceptible to attack (Entomology Today, 2014). 

Other Oleaceae species such as Osmanthus Lour., a 

genus of trees found in black water streams of the 

southern United States, remain virtually unstudied. 

While the susceptibility of other native Oleaceae to 

EAB is of no commercial relevance, it is a matter of 

considerable conservation significance. 

We suspect that modern systematic analyses 

employing molecular markers will reveal additional 

cryptic species that are ash specialists (especially 

in the western United States where species-level 

taxonomic studies lag). One interesting example 

that surfaced over the course of our studies involves 

the sizable and charismatic great sphinx (S. chersis). 

COI barcodes suggest the hawkmoth is two species, 

with the populations from southeastern Arizona 

representing an as yet undescribed species that 

Chris Schmidt (in litt.) believes is closely related to 

S. mexicana. Conversely, some taxa in our treatment 

may have been over split taxonomically. The mirid 

genus with 14 Tropidosteptes species is in need of 

revision, i.e., some names in Table 4 may prove to be 

synonyms (Michael Schwartz pers. comm.). 

In summary, we recognized 98 species of 

herbivores as being threatened by the loss of 

Fraxinus in the United States and Canada. No 

doubt, additional ash specialists will be identified 

in the coming decades. Knowledge of herbivores 

feeding on ash is severely lacking in the southern 

and western United States; very little is known of 

the phytophagous insects feeding on six western 

Fraxinus species (F. anomala, F. cuspidata, F. dipetala, 

F. gooddingii, F. greggii, and F. papillosa). Gall midges 

(Cecidomyiidae), curculionid weevils, mites, thrips, 

and other taxonomically challenging arthropods can 

be expected to yield additional Fraxinus specialists. 

The latter two taxa seem especially likely to include 

ash specialists because their taxonomy is nascent 

and no systematic continent-wide surveys have been 

carried out. Across all taxa, molecular markers can be 

expected to reveal new cryptic specialist herbivores, 

especially in those taxa where the species-level 

taxonomy has proven difficult. 

ConClUsion 

For the purposes of our ecological assessment we 

embraced the precautionary principle. The body of 

our assessment is, at its essence, a doomsday scenario: 

what might transpire if North America lost all of 

its Fraxinus or if ash numbers dwindled to a point 

where ash lost functional value in North American 

wildlands. Presently, EAB is spreading at a dramatic 

pace. We hope a growing number of parasitoids, 

pathogens, and predators will soon reduce the beetle’s 

hyperabundance and rate of spread, and that some 

subset of ash species, genotypes, age classes, etc. will 

prove resistant to EAB. However, should the beetle 

cause catastrophic losses of ash, as many as 150 U.S. 

plant community types (16 of which are regarded as 

imperiled or critically imperiled) could be severely 

compromised. Fraxinus has a surprisingly rich, 

specialized, beautiful, and noteworthy invertebrate 

fauna, including hercules beetles, rhinoceros 

beetles, and hawkmoths – some of our continent’s 

most magnificent invertebrates. By our assessment, 

the magnitude of North American invertebrate 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER 

50 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

biodiversity loss could greatly exceed that associated 

with American chestnut blight. The number of 

plant communities likely to be affected, the number 

of herbivores at risk (nearly 100 species), and the 

charismatic nature of the fauna in peril, argue for 

continued and increased efforts to bring the emerald 

ash borer under control. 

aCKnoWledgments 

This work is a compilation of the collective 

knowledge of more than 100 biologists, collectively 

representing >2500 person-years of accumulated 

study and knowledge, who made their expertise, 

and in some cases unpublished data, available to 

us. It was an honor to work with this august group. 

Botanists, forest managers, ecologists, and wildlife 

biologists – all of which are listed by name – are 

given in Appendices 1 and 2. Anton Reznicek, Jim 

Bissell, Jim McCormac, and Judy Semroc greatly 

shaped the content of what we present with regard to 

effects on plant communities and the likely cascading 

consequences of emerald ash borer. Principal 

authorities and sources for specialist herbivores are 

listed in Table 4. We are especially indebted to those 

who waded through multiple emails and reviewed 

preliminary lists. Roughly in order of deceasing 

email correspondence: Ray Gagné (Cecidomyiidae), 

John DeBenedictis (Yponomeutidae), Margarethe 

Brummerman (Dynastes), Tom Henry (Hemiptera), 

Rob Huber (Sesiidae), Charley Eisemen (leafminers, 

weevils), Jim Tuttle (Sphingidae), Charlie and 

Lois O’Brien (Curculionidae), Robert Anderson 

(Curculionidae), Michael Schwartz (Miridae), 

Rick Westcott (Coleoptera), Terry Fitzgerald 

(Gracillariidae), Shawn Clark (Chrysomelidae), 

David Smith (Tenthredinidae), and Laura Miller 

(Tingidae). Several colleagues and collectors 

supplied unpublished observations or data, especially 

Margarethe Brummerman, Ted MacRae, and Bill 

Warner. Roy Van Driesche, Faith Campbell, Tate 

Lavitt, Virginia Wagner, and David Cappaert made 

numerous helpful suggestions on drafts of the 

manuscript. Images were supplied by Daniel Boone, 

Margarethe Brummerman (2), Charley Eiseman, 

Tyger Gilbert (www.tygergilbert.com), Richard 

Hayes, Bill Johnson, Ken Metzler, Mike Quinn, 

Jim McCormac (3), Tom Murray, Anton Reznicek 

(2), Judy Semroc (4), and Tokyo Tower (Nippon 

Television City Corporation). Virge Kask helped with 

the preparation of figures. Support for this work, in 

part, was provided by USDA Forest Service FHTET 

Co-op Agreement 14-CA-11420004-138. Additional 

assistance came from a State Wildlife Grant from the 

Wildlife Division of the Connecticut Department of 

Environmental Protection. 

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56 

BIOLOGY AND CONTROL OF EMERALD ASH BORER APPENDIX 1. Contacted forest managers, plant ecologists, land managers, and wildlife biologists State Contact	 Affi liation CT-Department of Environmental Protection Connecticut	 May, Dale Delaware	 Tallamy, Doug Indiana	 Dunbar, Richard Homoya, Mike Shuey, John Michigan Kashian, Dan McCullough, Deb­ orah Reznicek, Anton 

Ohio	 Bissell, James 

Boone, Daniel Hausman, Constance Gardener, Richard McCormac, James Reinier, John Semroc, Judy 

Ontario Catling, Paul 

Gill, Bruce Oldham, Michael Waldron, Gary 

Wisconsin	 Wilterding, John 

(DEEP) University of Delaware Indiana Department of Natural Resources (INDNR)
Indiana Department of Natural Resources (INDNR)
Th e Nature Conservancy (TNC)
 Wayne State University
 Michigan State University 
University of Michigan
 Cleveland Museum of Natural History
 Bartlett Tree Experts
 Cleveland Metropolitan Park District
 Ohio Department of Natural Resources (ODNR)
 ODNR- Ohio Division of Wildlife
 Cleveland Metropolitan Park District
 Cleveland Museum of Natural History
 Agriculture and Agri-food Canada
 Canadian Food Inspection Agency
 Ontario Natural Heritage Information Centre 
(NHIC)
 University of Guelph
 Olivet College 

Area of Expertise/Comments

retired wildlife biologist; specialist on game speciesProfessor of Entomology and Wildlife Ecology; author of “Bringing Nature Home” Northeast Region Ecologist; Division of Nature PreservesBotanist; Division of Nature PreservesDirector of Conservation ScienceProfessor of Biological Sciences; forest ecologistProfessor of Entomology; forest entomologistAssistant Director of University of Michigan Herbarium; plant systematist; plant ecologistCurator of Botany; Coordinator of Natural Areas (50+ preserves)Certified arborist and field botanistPlant and Restoration EcologistChief Botanist (ODNR); ecologist non-game wildlife biologistWetland EcologistConservation SpecialistResearch Scientist; botanistResearch Scientist; entomologist; invasive species biologistBotanist; herpetologistSchool of Environmental Sciences; tree specialistProfessor of Biology and Chair of the Department of Natural and Physical Sciences; entomologist 

CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER
 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

BIOLOGY AND CONTROL OF EMERALD ASH BORER

APPENDIX 2. Contacted taxonomic authorities and principal experts for arthropod records.

Taxon Family Taxonomic Authority Affi liation	 Position/Area of Expertise

Systematic Entomology Lab, USDA Agriculture Acari Eriophyidae Ochua, Ron	 Research Entomologist Research Service (ARS)
 Systematic Entomology Lab, USDA Agriculture 
 Acari Tetranychidae Ochua, Ron	 Research Entomologist Research Service (ARS)
 Insect Museum, Oregon Department of Agricul- Museum Curator; Lead Taxonomic and Survey 
 Coleoptera Brentidae LaBonte, James ture	 Entomologist 

Senior Research Entomologist & Project Coleoptera Buprestidae MacRae, Ted Monsanto Company Leader 

Insect Pest Prevention & Management Program; Wescott, Rick	 Research Entomologist emeritus Oregon Department of Agriculture
 

Coleoptera Cerambycidae Alten, Ron N/A expert on western fauna


Systematic Entomology Lab, National Museum of 
 Lingafelter, Steven	 Research Entomologist Natural History, Smithsonian Institution 

Senior Research Entomologist & Project MacRae, Ted Monsanto Company Leader 

Monte L. Bean Life Science Museum, Brigham Coleoptera Chrysomelidae Clark, Shawn	 Entomology Collections Manager Young University 

Riley, Ed Texas A&M University Insect Collection Associate Curator 

Department of Entomology, National Museum of Staines, Charles 	 Research Entomologist Natural History, Smithsonian Institution
 

Sullivan, Patrick Th e Haden Collection, Sierra Vista, AZ Executive Curator 


Coleoptera Curculionidae Anderson, Robert Canadian Museum of Nature Research Scientist


Atkinson, Th omas Insect Collection, University of Texas, Austin Collections Manager
 

Department of Entomology, Texas A&M Univer-
 Burke, Horace R. 	 Professor emeritus sity
 Department of Entomology and Plant Pathology, 
 Clark, Wayne 	 Professor emeritus Auburn University 

 Cook Arthropod Research Collection, Michi-	 A.J. Associate Professor of Insect Systematics & Cognato, Anthony gan State University Research Collection Director

O’Brien, Charles W. University of Arizona Research Entomologist

Department of Entomology, National Museum of Coleoptera Hispinae Staines, Charles 	 Research Entomologist Natural History, Smithsonian Institution 

57 
 

58 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER
 APPENDIX 2. (continued) Taxon Family Taxonomic Authority Affi liation	 Position/Area of Expertise Systematic Research Collections, University of Coleoptera Scarabaeidae Ratcliff e, Brett	 Collection Curator, Professor of Entomology Nebraska State Museum Sullivan, Patrick Th e Haden Collection, Sierra Vista, AZ Executive Curator California State Collection of Arthropods, Warner, Bill	 California Department of Food and Agriculture Research Associate (CDFA) Department of Ecology and Evolutionary Biology, Coleoptera various Hespenheide, Henry	 Professor Emeritus University of California Los Angeles (UCLA) 

affi liate of Texas A&M, University of Texas at Quinn, Mike	 expert on Texas fauna Austin
 Center for Bottomland Hardwoods Research, 
 Schiff , Nathan 	 Research Entomologist USDA Forest Service Systematic Entomology Lab, USDA Agriculture Diptera Agromyzidae Scheff er, Sonja Jean 	 Molecular Systematist Research Service (ARS)
 Systematic Entomology Lab, National Museum of retired Research Entomologist, current Collab-
 Diptera Cecidomyiidae Gagné, Raymond Natural History, Smithsonian Institution orator 

Hemiptera Alyerodidae Creel, Debra USDA Agriculture Research Service (ARS) Museum SpecialistHemiptera Aphididae Blackman, Roger Natural History Museum, London Scientific Associate 

Systematic Entomology Lab, USDA Agriculture retired Research Entomologist, current Collab- Miller, Douglass Research Service (ARS)	 orator 

von Dohlen, Carol	 Utah State University Professor of Biology 

Systematic Entomology Lab, National Museum of Hemiptera Cicadellidae McKamey, Stuart 	 Research Entomologist Natural History, Smithsonian Institution
 

Hemiptera Coccoidea Normark, Benjamin University of Massachusetts, Amherst Professor of Biology
 

California Department of Food and Agriculture 
 Watson, Gillian 	 Senior Insect Biosystematist (CDFA)
 

Hemiptera Derbidae O’Brien, Lois University of Arizona systematist
 

Wilson, Stephen University of Central Missouri Professor of Biology
 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

BIOLOGY AND CONTROL OF EMERALD ASH BORER

APPENDIX 2. (continued) 

Taxon Family Taxonomic Authority Affi liation Position/Area of Expertise

Eastern Cereal and Oilseed Research Centre, Hemiptera Miridae Schwartz, Michael Research Entomologist Agriculture and Agri-Food Canada Systemic Entomology Lab, National Museum of Henry, Th omas Research Entomologist Natural History, Smithsonian Institution
 

Wheeler, Al Clemson University Adjunct Professor of Entomology


Hemiptera Pentatomidae Rider, Dave North Dakota State University Professor of Entomology


Subtropical Agriculture Research Center, USDA 
 Th omas, Donald Research Entomologist Agriculture Research Service (ARS)
 Systematic Entomology Lab, USDA Agriculture retired Research Entomologist, current Collab-
 Hemiptera Psyllidae Miller, Douglass Research Service (ARS) orator Systemic Entomology Lab, National Museum of Hemiptera Tingidae Henry, Th omas Research Entomologist Natural History, Smithsonian Institution Pest Identification Laboratory, West Virginia Miller, Laura Taxonomic Entomologist Department of Agriculture 

Wheeler, Al Clemson University Adjunct Professor of Entomology

Associate Professor of Entomology and Wild- Hemiptera various Bartlett, Charles University of Delaware life Ecology 

Systemic Entomology Lab, National Museum of retired Research Entomologist, current Collab- Hymenoptera Tenthredinidae Smith, David Natural History, Smithsonian Institution orator Systemic Entomology Lab, National Museum of Hymenoptera Eurytomidae Gates, Michael Research Entomologist Natural History, Smithsonian Institution 

Lepidoptera Geometridae McFarland, Noel N/A authority on life histories of western moths 


Rand, Evan N/A Arizona moth expert
 

National Museum of Natural History, Smithso-
 Lepidoptera Gracillariidae Davis, Don Curator nian Institution 

Distinguished Professor of Environmental Fitzgerald, Terry State University of New York (SUNY) at Cortland Sciences and Forestry

Follett Institute of Natural Sciences; University of Lepidoptera Noctuidae Quinter, Eric L. retired collection manager Connecticut affi liate 

59 
 

60 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER
 APPENDIX 2. (continued) Taxon Family Taxonomic Authority Affi liation Position/Area of Expertise Florida State Collection of Arthropods, Florida Lepidoptera Pyralidae Hayden, James Taxonomic Entomologist, Lepidoptera Curator Department of Agriculture
 Lepidoptera Sesiidae Hansen, Jason Michigan State University Research Scientist
 Canadian National Collection of Insects Canadi- systematist with Canadian Food Inspection Lepidoptera Sphingidae Schmidt, Chris an Food Inspection Agency, Ottawa Agency
 Tuttle, James P. N/A taxonomic expert
 Lepidoptera Yponomeutidae DeBenedictis, John Bohart Museum, University of California Davis Research Fellow
 Plant Pest Diagnostics Center, California Depart-
 Epstein, Marc Senior Insect Biosystematist ment of Food and Agriculture Canadian National Collection of Insects, Arach- Landry, Jean-Francois Taxonomic Entomologist nids and Nematodes Essig Museum of Biodiversity, University of Cali- Powell, Jerry fornia- Berkley Director Emeritus Department of Entomology, National Museum of Sohn, Jay Post-Doctoral Fellow Natural History, Smithsonian Institution
 

Lepidoptera various Jump, Peter N/A taxonomic expert 
Lepidoptera various Wagner, David University of Connecticut Professor of Ecology and Evolutionary BiologyLeafminers 
and Gall- various Eiseman, Charley N/A taxonomic expert 
Formers
 Th ysanoptera various Creel, Debra USDA Agriculture Research Service (ARS) Museum Specialist 

Department of Entomology, University of Califor- Th ysanoptera various Hoddle, Mark taxonomic expert nia at Riverside Ecosystem Sciences, Commonwealth Scientific Th ysanoptera various Mound, Laurence Honorary Research Fellow and Industrial Research Organisation (CSIRO) 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

BIOLOGY AND CONTROL OF EMERALD ASH BORER

APPENDIX 3. Misattributions from Published Literature and Online Sources

Previous Current Fraxinus Taxonomically Herbi- Native to Taxon Species Comment(s) Ranking Ranking Specialist? Valid? vore? U.S.? 

Invalid 	 Valid name: Aceria fraxini Acari Eriophyes fraxini Garm. High High Taxonomy	 (Baker et al., 1996) 

Polyphagous; hosts include Misattributed Tetranychus homorus High to 	 Carya, Fraxinus, Gossyp- Acari	 Not Imperiled Fraxinus Pritchard & Baker Moderate	 ium, and Poaceae (INRA, Specialist 2014) 

Misattributed	 Valid name: Ischyropalpus Anthicus nitidulus 	 Invalid Not an Coleoptera Moderate Not Imperiled Fraxinus	 nitidulus; mite predator LeConte	 Taxonomy Herbivore Specialist	 (Landwer, 1977) 

Valid name: Apion 

Misattributed cribricolle; recorded on Apion porosicolle	 Invalid Coleoptera High Not Imperiled Fraxinus	 deer weed, deer vetch, Gemm.	 Taxonomy Specialist	 wild buckwheat and Olea 

(Bright, 1993) Valid name: Linsleya sphaericollis; larvae feed 

Misattributed	 on grasshopper eggs, Invalid Coleoptera Lytta sphaericollis Say Moderate Not Imperiled Fraxinus	 adults on Fraxinus, lilac Taxonomy Specialist	 and honey suckle (Church 

and Gerber, 1977; Pinto and Bologna, 1999) No North American Misattributed cerambycids are known Coleoptera Obrium rufulum Gahan Moderate Not Imperiled Fraxinus to be ash specialists (Ted Specialist McCrae in litt.) 

Larvae feeds on Campsis radicans (Ed. Riley in litt.). 

Further Misattributed Adults oligophagous but Octotoma plicatula High to Coleoptera Research Fraxinus	 Fraxinus is a preferred (Fabricius) Moderate Required Specialist	 host; beetle population potentially impacted by EAB 

(Shawn Clark in litt.) 

61 
 

62 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER
 APPENDIX 3. (continued) Previous Current Fraxinus Taxonomically Herbi- Native to Taxon Species Comment(s) Ranking Ranking Specialist? Valid? vore? U.S.? Misattributed	 Valid name: Porricondyla Colpodia temeritatis	 Invalid Not an Diptera High Not Imperiled Fraxinus	 temeritatis; mycophagous Felt	 Taxonomy Herbivore Specialist	 (Raymond Gagné in litt.) Valid name: Contarinia Misattributed Continaria canadensis	 Invalid canadensis; contamination Diptera	 High Not Imperiled Fraxinus Felt	 Taxonomy record (Raymond Gagné, Specialist 1989; in litt.) Record from Solomon Invalid et al. (1993) refers to D. Diptera Dasineura spp. High High Taxonomy	 apicata; (Raymond Gagné in litt.). Valid name: Neolasioptera Misattributed Lasioptera fraxinifl ora 	 Invalid fraxinifolia; generalist, Diptera	 High Not Imperiled Fraxinus Felt	 Taxonomy contaminant (Raymond Specialist Gagné, 1989; in litt.) Misattributed Lestodiplosis fraxinifolia	 Not an Generalist predator (Ray- Diptera	 High Not Imperiled Fraxinus Felt	 Herbivore mond Gagné in litt.) Specialist 

Misattributed “Very definitely a general- Rhizomyia fraxinifolia Diptera High Not Imperiled Fraxinus 	 ist phyto- or saprophage” Felt Specialist	 (Raymond Gagné in litt.) 

“Feeds on a wide variety Misattributed Anormenis septentrion-	 of woody and herbaceous Hemiptera	 Moderate Not Imperiled Fraxinus alis (Spinola)	 plants” (Wilson and Specialist McPherson, 1981) 

Misattributed Hosts are Forestiera ligu- Leptoypha elliptica High- Hemiptera Not Imperiled Fraxinus	 strina and F. acuminata McAtee	 Moderate Specialist (Wheeler, 2002) 

Misattributed Hosts are Forestiera ligu- High to Hemiptera Leptoypha ilicis Drake Not Imperiled Fraxinus 	 strina and F. acuminata Moderate Specialist (Wheeler, 2002) Misattributed Hosts are Osmanthus and Leptoypha mcateei Hemiptera	 Moderate Not Imperiled Fraxinus Lyonia (Drake and Ruhoff , Drake Specialist	 1965) 
CHAPTER 2: ECOLOGICAL IMPACTS OF EMERALD ASH BORER

BIOLOGY AND CONTROL OF EMERALD ASH BORER

APPENDIX 3. (continued) 

Previous Current Fraxinus Taxonomically Herbi- Native to Taxon Species Comment(s) Ranking Ranking Specialist? Valid? vore? U.S.? 

Leptoypha nubilis High to High to Invalid Valid name: Leptoypha Hemiptera Drake Moderate Moderate Taxonomy minor 

Exotic/ In- Psyllopsis fraxinicola European species (Hod- Hemiptera High Not Imperiled troduced Forst. kinson, 1988) Species 

Th ysanocnemis bischoffi High to Invalid Valid name: Lignyodes Hemiptera High Blatchley Moderate Taxonomy bischoffi 

Th ysanocnemis helvola High to Invalid Valid name: Lignyodes Hemiptera High LeConte Moderate Taxonomy helvolus 

Wasps bulk reared & 

Misattributed only associated with ash; Hymenop- Not an Eurytoma spp. High Not Imperiled Fraxinus species likely parasitoid tera Herbivore Specialist (Keen, 1958; David Smith 

in litt.) 

Hymenop- Tethida cordigera Invalid High High Valid name: Tethida barda tera (Beauvois) Taxonomy
 

Neotropical species 
 Manduca brontes High to Extralimi- Lepidoptera Not Imperiled recorded from Jamaica (Drury) Moderate tal Species (Tuttle, 2007)
 

Color form of Podesia
 Misattributed Podosesia fraxini (Lug- Invalid syringa; oligophagous Lepidoptera Moderate Not Imperiled Fraxinus ger) Taxonomy (Eichlin and Duckworth, Specialist 1988) 

63 

65 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Chapter 3: Host Range and Host ResistanCe 

Daniel A. Herms 

Department of Entomology, The Ohio State University, Ohio Agricultural Research and Development Center, 

1680 Madison Ave., Wooster, Ohio 44691, herms.2@osu.edu

introdUCtion 

Since its discovery in North America in 2002, 

emerald ash borer (Agrilus planipennis Fairmaire) 

(EAB) has infested and killed many millions of ash 

trees (Fraxinus spp.) in forests, woodlots, urban 

forests, landscapes, and nurseries (Herms and 

McCullough, 2014). Ash species indigenous to 

eastern Asia share a coevolutionary history with 

EAB and are more resistant than evolutionarily 

naïve hosts indigenous to North America and 

Europe, presumably because they possess defenses 

targeted against EAB that have developed through 

natural selection (Wei et al., 2004, 2007; Liu et al., 

2007; Rebek et al., 2008). By 2010, EAB had killed 

more than 99% of white (F. americana L.), green (F. 

pennsylvanica Marsh.), and black (F. nigra Marsh.) ash 

in forests in southeast Michigan near the epicenter of 

the invasion, and seed production and new seedling 

germination had ceased (Kashian and Witter, 2011; 

Klooster et al., 2014). In the Moscow region of 

Russia, EAB is causing widespread mortality of 

European ash (F. excelsior L.) (Orlova-Bienkowskaja, 

2014), which also lacks a coevolutionary history 

with EAB. While buprestid wood-borers generally 

colonize only severely weakened or freshly killed trees 

(Evans et al. 2007), EAB is also killing healthy trees 

(Cappaert et al., 2005), making the invasions of North 

America and Russia especially devastating. 

host range oF emerald ash Borer 

Ash species indigenous to east Asia reported as hosts 

of EAB include Manchurian ash (F. mandshurica 

Rubr.) and two species of Chinese ash (F. chinensis 

Roxb. and F. rhyncophylla [Hance] A.E. Murray) (Wei 

et al., 2004, 2007) (of which the latter is sometimes 

given as a subspecies of F. chinensis) (Wallander, 

2001). These species are presumed to share a 

coevolutionary history with EAB (Liu et al., 2003, 

2007). 

In addition to white, green, and black ash, 

other species indigenous to North America that have 

been documented as hosts of EAB include pumpkin 

ash (F. profunda [Bush] Bush) (Knight et al., 2013), 

and blue ash (F. quadrangulata Michx.) (Anulewicz 

et al., 2008; Tanis and McCullough, 2012). Oregon 

ash (F. latifolia Benth.), native to the west coast of 

North America, was found to be highly susceptible 

in a common garden study conducted in southeast 

Michigan (Table 1). Velvet ash (F. velutina Torr.), 

native to the southwest United States and Mexico, has 

been colonized and killed by EAB when planted as 

an ornamental in China (Liu et al., 2003; Wang et al., 

2010), while freshly cut logs of Shamel (evergreen) 

ash (F. uhdei [Wenz.] Lingl.), which is indigenous to 

Mexico, were suitable for rearing emerald ash borer 

larvae in experimental studies (Duan et al., 2013). 

The susceptibility of Oregon, velvet, and Shamel ash 

suggests that the southwest and west coast of North 

America are vulnerable to EAB invasion, depending 

on the environmental tolerance of the insect. 

Some ash species and cultivars that are 

indigenous to Europe also have been confirmed 

as hosts for EAB (i.e., supporting successful larval 

development and adult emergence). Following this 

borer’s introduction to the Moscow region of Russia 

(Baranchikov et al., 2008), EAB caused widespread 

mortality of European ash (Orlova-Bienkowskaja, 

2014). In a common garden study in southeast 

Michigan, flowering ash (F. ornus L.), Raywood ash 

(F. angustifolia subsp. oxycarpa [M. Bieb. ex Willd.] 

Franco & Rocha Afonso [syn. F. oxycarpa M. Bieb. ex 

Willd.] cv. ‘Raywood’), and the European ash cultivar 

‘Aureafolia’ were readily colonized by EAB (Table 1). 
CHAPTER 3: HOST RANGE AND HOST RESISTANCE

66 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

Table 1. Survival and canopy condition of ash species and cultivars in 2009, 2011, and 2014 in a common garden established in southeast Michigan in 2004. Canopies of living trees were rated on a scale of 1 

(severe decline) to 5 (no decline). Each taxon was replicated 20 times in a randomized complete block 

design. 

Species Cultivar Geographic 

Origin 

2009 2011 2014 

% Survival Canopy 

Rating 

% Survival Canopy 

Rating 

% Survival Canopy 

Rating 

F. mandshurica seedling origin Asia 85 4.6 80 4.80 80 4.20 

F. nigra x mandshurica Northern 

Treasure 

Asia x North 

America hybrid 

90 4.4 80 4.80 80 4.00 

F. excelsior Aureafolia Europe 25 3.8 10 5.00 5 2.00 

F. ornus seedling origin Europe 20 1.5 0 NA 0 0.00 

F. angustifolia

subsp. oxycarpa 

Raywood Europe 35 4.8 30 3.60 0 NA 

F. americana Autumn Applause North America 40 4.4 25 4.60 20 2.00 

F. americana Autumn 

Purple 

North America 50 4.6 50 4.60 40 2.10 

F. americana seedling origin North America 85 4.8 70 4.10 45 2.90 

F. americana Sparticus North America 55 4.9 45 4.90 45 2.10 

F. latifolia seedling origin North America 25 2.3 5 2.00 0 NA 

F. nigra Fallgold North America 35 4.5 15 2.70 5 3.00 

F. nigra seedling origin North America 10 5.0 5 5.00 0 NA 

F. pennsylvanica Cimmaron North America 40 5.0 40 4.90 35 2.90 

F. pennsylvanica Patmore North America 30 5.0 30 4.40 15 2.30 

F. pennsylvanica Summit North America 20 20.0 15 3.30 0 NA 

F. quadrangulata seedling origin North America 90 4.8 80 4.60 65 2.20 

In Japan, species of Juglans (walnuts and 

butternuts), Ulmus (elms), and Pterocarya (wingnuts) 

have been reported as hosts for EAB (Haack et al., 

2002). However, EAB has not been well studied 

in Japan, and host records for wood-borers can be 

unreliable, potentially including species from which 

adults were collected even when they do not colonize 

that species in the larval stage, or they may represent 

taxonomic errors or confusion (e.g. synonymy of 

separate species) (Muilenburg and Herms, 2012; 

Haack, 2013). In experimental host range studies, 

EAB larvae were not able to complete development 

on American elm (Ulmus americana L.), black walnut 

(Juglans nigra L.), hackberry (Celtis occidentalis L.), 

shagbark hickory (Carya ovata [Mill.] K. Koch), or on 

members of the ash family (Oleaceae) tested, including 

Japanese tree lilac (Syringa reticulata Bl.), swamp privet 

(Forestiera acuminata [Michx.] Poir.), Chinese privet 

(Ligustrum sinense Lour.), and glossy privet (Ligustrum 

lucidum Ait.) (Anulewicz et al., 2006, 2007). Recently, 

white fringe tree (Chionanthus virginicus L.), which is 

also in the ash family, was confirmed as a larval host 

for EAB (Cipollini, 2015). 

interspeCiFiC patterns oF ash 

resistanCe to eaB 

Emerald ash borer is only occasionally a damaging 

pest of ash species native to eastern Asia, but has 

caused widespread mortality of North American ash 

species planted in China (Wei et al., 2004, 2007). For 

example, EAB killed all white ash trees planted in 
CHAPTER 3: HOST RANGE AND HOST RESISTANCE

67 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

the city of Shenyang, as well as all trees in a 10-yearold white ash planting in the experimental forest 

of Northeast Forestry University in Harbin. The 

outbreaks occurred at the same time EAB populations 

were low on Manchurian ash in neighboring forests. 

In another study, Liu et al. (2007) observed that green 

ash was colonized at a higher rate than native Asian 

species planted at the same site. They concluded 

based on their field surveys that EAB does not pose 

a serious threat in China to indigenous ash species. 

However, Liu et al. (2003) and Wei et al. (2004, 2007) 

reported that white ash is no longer planted in China 

and plantings of green ash remain only in localized 

areas because of past EAB attack. The EAB invasion 

of Russia west of the Urals has made it apparent 

that European ash is also highly susceptible to EAB 

(Orlova-Bienkowskaja, 2014). 

Colonization of Asian ash species by EAB has 

been consistently associated with stressed and dying 

trees (Wei et al. 2004, 2007; Liu et al. 2007), which 

suggests that they may be inherently resistant and 

that EAB has evolved as a secondary colonizer of 

stressed trees, as is the case with many species of 

Buprestidae (Evans et al. 2007). Experimental studies 

of EAB adult host preference and larval performance 

are consistent with this hypothesis. For example, 

EAB adults preferred to feed upon foliage from leaves 

from trees stressed by girdling (Chen and Poland, 

2009), injured by adult feeding damage, or induced 

by methyl jasmonate (Rodriguez-Saona et al., 2006). 

In field experiments, adult-landing rates were higher 

on girdled trees, as were larval densities and growth 

rates (McCullough et al., 2009; Tluczek et al., 2011). 

Jennings et al. (2014) found that females preferred 

to oviposit on declining trees that were previously 

infested by EAB rather than on healthy trees. 

All North American ash species encountered 

to date by EAB have proven susceptible to varying 

degrees (Herms and McCullough, 2014). Black, 

green, and white ash are highly susceptible (Klooster 

et al., 2014), although white ash is somewhat less 

preferred, possibly because its smoother bark (at 

least in younger trees) may be a less preferred 

oviposition substrate (Anulewicz et al., 2008). In 

forests, trees with rougher bark were reported to be 

killed at a slightly faster rate than smoother barked 

trees (Marshall et al., 2013). However, at the stand 

level, black, white, and green ash declined at similar 

rates, with populations of all three species ultimately 

reaching greater than 99% mortality at about the 

same time (Smith, 2006; Smith et al., 2015; Klooster 

et al., 2014). Blue ash (F. quadrangulata) appears to 

be the least vulnerable North American ash species 

encountered by EAB to date. Tanis and McCullough 

(2012) observed that more than 60% of blue ash in 

wooded areas in southeastern Michigan appeared 

healthy, while white ash with trunks greater than 10 

cm in diameter were all killed. 

Patterns of ash decline and mortality in an ongoing common garden study established at Michigan 

State University’s Tollgate Education Center in 

Novi, Michigan in 2004 are largely consistent with 

the hypothesis that coevolved species indigenous 

to Asia are more resistant than evolutionary naïve 

hosts native to North America and Europe (Table 

1). The resident EAB population was low when the 

plot was established as most trees in the region had 

been killed. As EAB populations began to resurge 

and susceptible trees in the plot began to be killed, 

Manchurian ash had the highest rate of survival 

and little canopy decline. Mortality of Manchurian 

ash that did occur was concentrated in the first few 

years after planting, perhaps due to transplant stress. 

The only tree killed after 2009 had its trunk badly 

injured by a deer rub. The high EAB resistance of 

this Manchurian ash population of seedling origin is 

consistent with that observed by Rebek et al. (2008) 

for the clonal Manchurian ash cultivar ‘Mancana,’ 

suggesting that EAB resistance is a species-level trait. 

Fraxinus x ‘Northern Treasure’ ash, which is a 

Manchurian (Asian) x black ash (North American) 

hybrid (Davidson, 1999) had similarly high survival 

and low canopy decline, suggesting introgression 

of Manchurian ash resistance genes into the hybrid 

(Table 1). However, this pattern contrasts sharply 

with that observed by Rebek et al. (2008), who found 

‘Northern Treasure’ ash to be highly susceptible to 

EAB. This suggests there is taxonomic confusion in 

the nursery industry surrounding this cultivar that 

has yet to be resolved. 

Most North American species and cultivars in 

the common garden study experienced substantial 
CHAPTER 3: HOST RANGE AND HOST RESISTANCE

68 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

mortality, with green ash cultivars, black ash, and 

Oregon ash declining more rapidly than white ash 

cultivars (Table 1). Blue ash has survived at a higher 

rate than other North American species, but by 2014 

had lower survival and greater canopy decline than 

Manchurian ash. Furthermore, decline and mortality 

of blue ash increased over time, suggesting that 

surviving trees may continue to succumb to EAB as 

other hosts are eliminated. The European species 

and cultivars evaluated in the common garden also 

experienced high decline and mortality, including 

F. ornus, F. excelsior ‘Aureafolia’, and F. angustifolia 

subsp. oxycarpa ‘Raywood’ (Table 1). 

The high level of resistance of Asian ash relative 

to North American and European species has 

been attributed to a coevolutionary history that 

has stabilized the interaction between EAB and its 

indigenous hosts in Asia (Liu et al., 2003, 2007; Rebek 

et al., 2008). Conversely, the widespread mortality of 

Nearctic and European ash species in invaded regions 

has been attributed to very high susceptibility of 

evolutionarily naïve host plants, which has facilitated 

the spread and population growth of EAB in defensefree space (Gandhi and Herms, 2010; Raupp et al., 

2010). A similar pattern has been observed for birch 

(Betula spp.) resistance to congeneric bronze birch 

borer (Agrilus anxius Gory), which is endemic to 

North America. North American birch (Betula) 

species share a coevolutionary history with bronze 

birch borer and are much more resistant than 

evolutionarily naïve Eurasian birch species (Nielsen et 

al., 2011). 

meChanisms oF resistanCe 

oF ash to eaB 

Host plant resistance to insects is considered a 

continuous trait ranging from complete immunity at 

one end of the spectrum to extreme susceptibility at 

the other (Painter, 1958; Beck, 1965). Mechanisms of 

resistance have been broadly classified as antibiosis 

(plants traits that lower herbivore performance, 

including fecundity, growth, and survival), 

antixenosis (plant traits that reduce behavioral 

preferences for feeding or oviposition), and tolerance 

(traits that allow a plant to grow or repair injury to 

a greater degree than another host experiencing the 

same amount of herbivory) (Painter, 1958; Beck, 

1965; Wiseman, 1985). Biogeographically, resistance 

has been classified as coevolved (host defenses 

resulting from natural selection) or allopatric 

(herbivore lacks the pre-adaptions needed to perform 

well on a novel host) (Harris, 1975). 

Because the devastating impact of EAB on its 

host is due to larval feeding, research on mechanisms 

of resistance have focused on factors affecting larval 

density and survival, including traits affecting female 

fecundity and oviposition preferences, as well as stem 

defenses and nutritional quality that influence larval 

establishment, growth, and survival. However, the 

relative importance of antibiosis and antixenosis in 

inter- or intraspecific variation in resistance of ash 

to EAB has yet to be fully delineated, and the role of 

tolerance has not been investigated. 

EAB adults have demonstrated variation in host 

preference for maturation feeding and oviposition. 

Pureswaran and Poland (2009) found that adults 

preferred to feed on green, black, and white ash 

relative to Manchurian, blue, and European ash. 

This pattern corresponds largely with patterns of 

resistance and vulnerability observed in the field, 

with the most susceptible species also being preferred 

(with the exception of European ash, which is highly 

susceptible), and suggests that there might be general 

correspondence between adult feeding preferences 

and female oviposition preferences. Consistent with 

this hypothesis, Rigsby et al. (2014) observed in two 

common garden experiments that females oviposited 

much more extensively on white and green ash than 

on Manchurian ash, and Anulewicz et al. (2008) 

found that females preferred to oviposit on green and 

white ash relative to blue ash. These findings also 

suggest that oviposition preference is an important 

determinant of interspecific variation in ash mortality 

and decline observed in field studies. 

Mechanisms of tree resistance to wood-borer 

larval feeding are not well understood but have been 

postulated to result from integrated constitutive and 

induced physical and chemical defenses of the phloem 

and outer xylem (Matson and Hain, 1985; Dunn et 

al., 1990; Muilenburg and Herms, 2012). Studies to 

elucidate the mechanism of resistance of Manchurian 
CHAPTER 3: HOST RANGE AND HOST RESISTANCE

69 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

 

 

 

 

ash to EAB have focused on comparing its induced and 

constitutive phloem chemistry to that of susceptible 

species. Eyles et al. (2007) compared the constitutive 

phloem phenolic chemistry of dormant stems of 

Manchurian, white, and green ash and identified 

compounds present in the Manchurian ash cultivar 

‘Mancana’ that were not present in the more susceptible 

species, including several hydroxycoumarins and 

two phenylethanoids (calceolariosides A and B) 

and suggested they might represent potential EAB 

resistance mechanisms. In a similar analysis conducted 

during the growing season, Cipollini et al. (2011) also 

found the constitutive phenolic profile of Manchurian 

to be distinctly different from that of green and white 

ash, observing patterns of qualitative variation similar 

to those reported by Eyles et al. (2007). 

In more phylogenetically controlled comparisons, 

however, Whitehill et al. (2012) detected these putative 

resistance compounds in concentrations comparable to 

or higher in highly susceptible black and European ash, 

which are much more closely related to Manchurian 

ash than are green and white ash. This strongly 

suggests that hydroxycoumarins and calceolariosides 

A and B are, in fact, not responsible for the high 

resistance of Manchurian ash. Pinoresinol dihexoside 

and a tentatively identified coumarin derivative were 

the only phenolic compounds detected that were 

unique to Manchurian ash, which suggests that the 

other 25 phenolic compounds detected are unlikely 

to play a role in resistance unless they synergize other 

classes of compounds that are unique to Manchurian 

ash (Whitehill et al., 2012). They did speculate that 

that two unique lignans may serve as markers for, or 

contribute directly to, the higher EAB resistance of 

Manchurian ash (Whitehill et al., 2012). They also 

proposed that the very distinct phenolic profile of blue 

ash may contribute to its higher level of resistance to 

EAB relative to green and white ash. 

The constitutive protein chemistry of ash phloem 

also has been examined. Manchurian ash had higher 

soluble protein concentration and a higher rate of 

browning (oxidation) reaction than did green or white 

ash, although trypsin inhibitor activity, peroxidase 

activity, and total soluble phenolic concentrations 

of Manchurian ash were lower than in at least one 

of the more susceptible species (Cipollini et al., 

2011). Whitehill et al. (2011) compared the phloem 

proteomes of Manchurian, black, green, and white 

ash, and they identified several proteins implicated 

as defenses in other species that were constitutively 

over-expressed in Manchurian ash relative to the other 

species and might contribute to resistance. These 

include a PR-10 protein, phenylcoumarin benzylic 

ether reductase, an aspartic protease, and ascorbate 

peroxidase. 

Nutritional quality of plants also contributes 

to variation in their resistance to herbivores, and 

Hill et al. (2012) quantified phloem compounds in 

Manchurian, green, and white ash that are thought to 

be of nutritional significance to EAB larvae, including 

nitrogen, total protein, free amino acids, total soluble 

sugars, and macro- and micro-nutrients. They found 

few differences, although concentrations of the amino 

acid proline, as well as the amino acid derivatives 

tyramine and tyrosol were higher in Manchurian ash. 

Chen et al. (2011) reported that larval growth was 

reduced on artificial diets in which protein or amino 

acids were limiting, and that the downward orientation 

of feeding as larvae formed their galleries allowed them 

to consume phloem with higher water and essential 

amino acid concentrations. 

Chakraborty et al. (2014) examined induced 

responses of Manchurian and black ash phloem to 

larval feeding, which has received far less attention 

than constitutive patterns. They found that EAB larval 

biomass was lower on Manchurian ash, which provides 

evidence that antibiosis as well as ovipositional 

non-preference contributes to high resistance of 

Manchurian ash, as does the observation of Duan et al. 

(2012) that host plant factors caused higher mortality 

of larvae feeding on Asian species of ash than on North 

American green ash. EAB larval feeding induced 

higher concentrations of pinoresinal A in Manchurian 

than black ash, which Chakraborty et al. (2014) 

speculated might contribute to resistance. Drought 

stress increased larval performance on both species, 

which is consistent with the hypothesis that stress 

increases host quality. 

Counter adaptations of EAB larvae to ash defenses 

have also been examined. Transcriptomic studies of 

EAB have focused on larval enzymes that function in 

detoxification of host defenses (Rajarapu et al., 2011; 
CHAPTER 3: HOST RANGE AND HOST RESISTANCE

70 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

 

 

 

 

 

 

Rajarapu and Mittapalli, 2013). Chen et al. (2012) 

found that phenolic concentrations were lower in EAB 

frass than in phloem tissue and inferred that larvae 

may excrete phenolics and/or convert them to nonphenolic compounds before excretion. 

Breeding For resistanCe to eaB 

Because of their inherent resistance to EAB, Asian 

ash species are a likely source of resistance genes 

that might be introgressed into North American 

species (Whitehill et al., 2011), and efforts to breed 

EAB-resistant ash are ongoing (Koch et al., 2012). 

Extensive surveys of ash stands in Michigan and Ohio 

have revealed a very small proportion of ash that 

remain healthy where EAB-ash induced mortality 

exceeds 99%, and thus may provide a potential 

source of allopatric resistance genes in native ash 

populations (Knight et al., 2012). However, it 

remains to be documented whether these genotypes 

are truly resistant or just lucky. Genomic sequencing 

of Asian and North American ash species have also 

been conducted to provide a molecular foundation 

for targeted breeding (Bai et al., 2011; Rivera-Vega et 

al., 2012) that ultimately may lead to restoration of 

ash to urban and natural forests of North America. 

aCKnoWledgements 

David Smitley (Department of Entomology, Michigan 

State University) and Bert Cregg (Department of 

Horticulture, Michigan State University) and their 

laboratory groups helped with establishment of 

the ash common garden study at the Michigan 

State University Tollgate Education Center in 

Novi, Michigan. Roy Prentiss, Farm Manager at 

the Tollgate Education Center, provided excellent 

support in the establishment and maintenance of the 

plantation. This work was funded by USDA APHIS 

and USDA Forest Service Northern Research Station, 

as well as by state and federal funds appropriated to 

The Ohio State University and the Ohio Agricultural 

Research and Development Center. 

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Chapter 4: other options For emerald ash Borer management: 

eradiCation and ChemiCal Control 

Deborah G. McCullough 

Department of Entomology & Department of Forestry, Michigan State University, East Lansing, Michigan 48824 

mccullo6@mail.msu.edu 

the early years — CoUld eaB have 

Been Contained or eradiCated? 

Following identification of emerald ash borer (Agrilus 

planipennis Fairmaire) (EAB) (Coleop.: Buprestidae) 

in Michigan in July 2002, state and federal regulatory 

officials began surveys to delimit the infestated area 

in the greater Detroit area (Cappaert et al., 2005; 

Herms and McCullough, 2014). It rapidly became 

clear that EAB was causing substantial ash mortality 

and decline, but there was little information available 

on even basic aspects of EAB biology. No species of 

Agrilus beetles were known to produce long range sex 

or aggregation pheromones, and there were certainly 

no traps or lures available for EAB surveys. A high 

proportion of ash in the suburban municipalities 

northwest of Detroit was dead or dying, so regulatory 

personnel conducted visual surveys along transects 

radiating out from the known infestation. Survey 

crews checked ash trees for symptoms such as 

canopy dieback, bark cracks (revealing EAB larval 

galleries), and epicormic sprouts on large branches 

or the trunks of infested trees. By autumn 2003, six 

counties in southeast Michigan were quarantined 

and at the time, regulatory officials believed the 

quarantine boundaries extended well beyond the 

actual infestation (Cappaert et al., 2005; Poland and 

McCullough, 2006; Siegert et al., 2014). 

Along with visual surveys, officials in Michigan 

initiated trace-backs and trace forwards in 2002 and 

2003 to track ash nursery trees shipped from the 

infested area. Ash, primarily cultivars of green ash 

(Fraxinus pennsylvanica Marshall) and white ash (F. 

americana L.) were abundant in most commercial 

nurseries in southeast Michigan when EAB was 

identified. Ash species were popular because they 

tolerate the often stressful conditions found in urban 

environments (Schoon, 1993; MacFarlane and Meyer, 

2005; Poland and McCullough, 2006) and were 

commonly planted in commercial landscapes, along 

roads and highways, as well as on private residential 

property. Ash trees near sawmills that processed 

ash logs, along with ash in campgrounds and tourist 

destinations likely to attract people with firewood, 

were also intensively surveyed. 

Eradication of EAB within the six counties in 

southeast Michigan was never considered a realistic 

option, given the millions of ash trees in urban, 

residential, and forested areas and the geographic 

extent of the infestation. Landscapers had begun 

treating some declining ash trees in the Detroit area 

with insecticides even before EAB was identified in 

2002. Treatment efficacy varied but none provided 

100% control (McCullough et al., 2005, 2006; Herms 

et al. 2014). Moreover, there were no practical or 

economically feasible means to treat the millions of 

ash trees growing in the affected areas (Cappaert et 

al., 2005; Herms and McCullough, 2014). 

It was clear, however, that continued spread of 

EAB would threaten more than 8 billion ash in U.S. 

forests along with millions of ash in urban landscapes. 

A strategy similar to that applied to large wildfires 

was proposed by scientists and regulatory officials 

appointed to the EAB Science Advisory Panel. Nearly 

complete mortality of ash within the infested area, 

which was already underway, would eventually lead 

to a substantial drop in EAB density in the core of 

the infestation and over time, the severely affected 

area would expand. If the advancing front of the 

infestation could be contained or at least slowed 

below the rate at which the core expanded, the EAB 

population would presumably collapse as fewer and 
CHAPTER 4: OTHER OPTIONS FOR EAB MANAGEMENT: ERADICATION AND CHEMICAL CONTROL

76 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

fewer host trees became available. Regulations to 

restrict transport of ash trees, logs, firewood, and 

related materials out of the quarantined area were 

part of the effort to contain the infestation (Federal 

Register, 2003; Herms and McCullough, 2014). 

Officials initially considered removing ash trees 

in a 5-10 km band around the infested area to deplete 

potential hosts for dispersing EAB adults. This strategy, 

referred to as a firebreak or an ash-free zone (Herms 

and McCullough, 2014), was never attempted in 

the United States. As surveys continued, the extent 

of the main EAB infestation in southeast Michigan 

and northwest Ohio became apparent. Officials 

realized that the inability to accurately delineate the 

infestation, the logistical problems of establishing an 

ash-free band, and the costs of creating such a band 

were insurmountable. Canadian officials did attempt 

to establish an ash-free zone in Ontario in 2004, but 

infested trees were soon found beyond this zone and 

the firebreak idea was abandoned. 

Along with efforts to contain or slow expansion 

of the main EAB infestation, officials determined that 

localized “outlier” infestations beyond the quarantine 

zone would be aggressively treated with the goal 

of eradication. These satellite populations of EAB, 

often referred to as “outliers,” originated from long 

distance transport of infested ash nursery trees, logs, 

or firewood. Large scale field studies that involved 

systematically felling and debarking ash trees around 

a known origin showed that while EAB females laid 

eggs on trees at least 750 m from their emergence 

point, most eggs were laid within 100 m of the adult 

beetles’ emergence point (Mercader et al., 2009; 

Siegert et al., 2010). Regulatory officials determined 

that eradication projects would encompass an area 

bounded by a perimeter 800 m beyond the furthest ash 

tree known to be infested. This distance represented 

a compromise between the need to eliminate 

infested but non-symptomatic trees and logistical 

and economic constraints associated with such a 

substantial undertaking (Herms and McCullough, 

2014). Within the eradication project area, every 

ash tree greater than 2.5 cm in diameter was felled, 

sectioned and transported to a disposal yard where 

the material could be chipped. Numerous outlier 

sites, primarily in Michigan, Ohio, and Indiana, 

were targets for eradication between 2003 and 2006 

(Cappaert et al., 2005; Herms and McCullough, 2014). 

The most extensive EAB eradication project occurred 

in Maryland, where more than 42,000 ash trees were 

removed between 2003 and 2009 across an area that 

eventually encompassed nearly 70 km2

 (MD-DNR, 

2014). 

Eradication efforts, with the exception of 

Maryland, were abandoned in 2006, in part because 

funds for eradication, surveys, and related activities 

were decreasing, but also because outlier populations of 

EAB continued to be found well beyond the quarantine 

boundaries (GAO, 2006; Herms and McCullough, 

2014). Between 2004-2006, state regulatory officials 

in Michigan, Indiana and Ohio established grids of 

small (≈ 15 cm diameter) ash detection trees, typically 

in right-of-ways along highways and roads (Rauscher, 

2006; Hunt, 2007). These trees were girdled in spring, 

making them highly attractive to adult EAB during the 

summer, then were debarked in autumn or winter to 

determine if larvae were present (McCullough et al., 

2009). Using girdled trees, along with increased public 

awareness of EAB, led to the identification of several 

previously unknown EAB infestations. 

As scientists learned more about EAB, it became 

clear that visual surveys to identify infested trees 

for detection or to delineate an infestation were 

inadequate. External evidence of EAB infestation is 

not apparent until larval densities reach moderate 

or high levels, while recently infested trees with low 

larval densities exhibit few, if any, symptoms (Poland 

and McCullough, 2006; Poland et al., 2011). Moreover, 

in relatively healthy trees, most EAB larvae require 

two years to complete development (Siegert et al., 

2010; Tluczek et al., 2011). Therefore, trees are usually 

infested for at least 3-4 years before any external 

symptoms become apparent. More recent evidence also 

suggests a small proportion of mature, mated females 

likely disperse relatively long distances, despite an 

abundance of suitable host trees in the local vicinity 

(McCullough et al., 2011a; Mercader et al., 2012), 

contributing to the difficulty of delineating or detecting 

new infestations. Eradication activities undoubtedly 

eliminated a very high proportion of infested trees 

and developing larvae, but it remains unclear as to 

whether any projects were successful. Infestations near 
CHAPTER 4: OTHER OPTIONS FOR EAB MANAGEMENT: ERADICATION AND CHEMICAL CONTROL

77 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

eradication areas could represent reproduction by EAB 

that had already dispersed beyond the boundaries of 

a project area or may reflect subsequent expansion or 

immigration of beetles from other populations (Herms 

and McCullough, 2014). 

systemiC inseCtiCides, eaB, 

and ash trees 

Once eradication efforts ceased, landowners and 

residents were left to deal with ash trees and EAB on 

their own. Early studies soon after EAB was identified 

in North America showed spraying the foliage and 

upper canopy of landscape trees with relatively 

persistent insecticides (e.g., bifenthrin, cyfluthrin) 

could effectively control adult EAB and protect trees 

(McCullough et al., 2005, Herms et al., 2014). Sprays 

were not popular, however, because of problems such 

as drift and possible environmental contamination, 

potential effects on non-target organisms such as 

pollinators and beneficial predatory insects, and 

possible applicator exposure. In addition, adequate 

coverage of the upper canopy of large trees was difficult 

and trees in many locations could not be reached with 

spray equipment. 

Fortunately, options for protecting landscape 

ash trees in urban areas from EAB have progressed 

substantially in the past decade. Systemic insecticides 

are now used to treat the vast majority of ash trees in 

urban areas where EAB is present. These products 

are applied by injecting the insecticide into the outer 

sapwood (xylem) around the base of the trunk of 

the tree (e.g., emamectin benzoate, imidacloprid, 

azadiractin) or applying it to the soil around the base 

of the tree for uptake by roots (e.g., dinotefuran, 

imidacloprid) (Herms et al., 2014). Products with 

dinotefuran, a highly soluble compound, can also 

be applied as a basal trunk spray (McCullough et 

al., 2011b; Herms et al., 2014). Trees transport the 

insecticide in xylem tissue from the base of the tree up 

to branches and foliage in the canopy (Sur and Stork, 

2003; Mota-Sanchez et al., 2009; Tanis et al., 2012). 

Systemic products eliminate most problems associated 

with cover sprays of insecticides. They must be applied, 

however, before high densities of EAB larvae injure the 

vascular system of an ash tree (Herms et al., 2014). 

When EAB was first identified, only a few 

systemic insecticide products were available. 

Imidacloprid was the active ingredient in most 

of those products and was applied either as a soil 

drench or by injecting the product into the base of 

the tree. Field trials with these products, however, 

yielded inconsistent results (McCullough et al., 

2006; Herms et al., 2014). Products protected trees 

from EAB injury in some sites, but in other sites, the 

same treatments were not effective. In some studies, 

EAB damage continued to increase, despite annual 

insecticide applications. Treated trees sometimes 

lived a few years longer than untreated trees, but 

still succumbed to EAB, despite the investment in 

treatment (McCullough et al., 2006). 

Research continued and new systemic 

insecticides became available, application technology 

improved, and our understanding of how to optimize 

these treatments advanced considerably. A product 

with the active ingredient emamectin benzoate, first 

registered in the United States in 2010, is the most 

effective systemic insecticide currently available for 

EAB control (Smitley et al., 2010; McCullough et al., 

2011b; Herms et al., 2014). Many field trials showed 

that emamectin benzoate consistently provided 

2-3 years of nearly complete EAB control, even 

when local EAB densities were high (Smitley et al. , 

2010; McCullough et al., 2011b; Herms et al., 2014). 

Many cities in the United States, as well as private 

landowners, are now protecting valuable ash trees 

from EAB with this product. Economic analyses 

showed costs of protecting landscape trees with the 

emamectin benzoate product to be substantially 

lower over time than the costs of removing trees 

killed by EAB (McCullough and Mercader, 2012; 

Van Atta et al., 2012). Treating a portion of the trees 

may also slow the rate of EAB population growth in a 

localized area (Mercader et al., 2011a,b; McCullough 

and Mercader, 2012). Insecticides with azadirachtin, a 

compound derived from the neem tree (Azadirachta 

indica A. Juss.) as the active ingredient, have recently 

become available for EAB control (McKenzie et 

al., 2010; Herms et al., 2014) in the United States 

and Canada and provide 1-2 years of protection, 

depending on local EAB density. Unlike other 

insecticides, which are toxic to EAB adults and larvae, 
CHAPTER 4: OTHER OPTIONS FOR EAB MANAGEMENT: ERADICATION AND CHEMICAL CONTROL

78 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

azadirachtin products affect EAB reproduction and 

development of young larvae (McKenzie et al., 2010; 

Kreutzweiser et al. 2011, DGM, unpubl. data). Basal 

trunk sprays of dinotefuran, a highly soluble “new 

generation” neonicointoid product, are effective if 

applied annually and are popular among arborists, 

especially when many small trees require treatment 

(McCullough et al., 2011b; Herms et al., 2014). 

Dinotefuran sprayed on the trunk moves through 

the outer bark and into the xylem, where it is then 

transported to the canopy. Imidacloprid insecticides, 

which also must be applied annually, continue to be 

used for EAB control, although effectiveness of these 

products varies considerably (Herms et al., 2014). 

integrating systemiC inseCtiCides 

and BiologiCal Control 

It is important to note that biological control and 

systemic insecticides are not mutually exclusive 

and in combination may yield additive or even 

synergistic (e.g., superadditive) effects on EAB 

population growth (Barclay and Li, 1991; Berec et 

al., 2007; Suckling et al., 2012). Simulations have 

shown that decreasing pest density with a densityindependent tactic such as systemic insecticides 

may enhance the effectiveness of density-dependent 

tactics, including biological control, particularly if a 

parasitoid displays nonrandom searching behavior 

(Barclay and Li, 1991; Suckling et al., 2012). Larval 

parasitoids and woodpeckers will not attack dead 

EAB larvae. Thus, unlike cover sprays, which are 

likely to affect a wide range of natural enemies, 

systemic products should have negligible effects on 

populations of native or introduced parasitoids (or 

predators) of EAB. Minimally, an additive effect 

should occur because systemic insecticides and 

biological control agents target different life stages 

of EAB. Systemic insecticides affect adult beetles 

as they feed on leaves and control newly hatched, 

neonate larvae, whereas native and introduced EAB 

parasitoids attack EAB eggs or late instar larvae. 

A synergistic effect may occur if untreated trees 

near trees treated with the emamectin benzoate 

product benefit from lower local EAB populations 

(McCullough and Mercader, 2012). Such trees would 

provide a consistent, multi-year source of EAB eggs 

and larvae to retain and support parasitoids. A similar 

interaction may occur in areas where the native ash 

species demonstrate some level of resistance to EAB. 

Black ash (Fraxinus nigra Marshall) and green ash, 

for example, are highly attractive and vulnerable 

hosts for EAB, white ash is intermediate, but healthy 

blue ash (Fraxinus quadrangulata Michx.) trees do 

exhibit resistance (Cappaert et al., 2005; Anulewicz 

et al., 2007; Limback, 2010; Tanis and McCullough, 

2012). Interactions between parasitoids and EAB 

in areas where a portion of ash trees are protected 

with effective systemic insecticides or in sites 

with relatively resistant ash species remain to be 

determined. 

FeWer options to proteCt ash 

trees in Forests 

While landscape trees can now be effectively treated 

with systemic insecticides, these products are not 

practical options for ash trees in forests, woodlots, 

riparian zones, or other natural areas. In part, this 

reflects the substantially higher economic value of 

individual urban landscape trees compared to forest 

trees. Many practical and environmental concerns 

also limit the use of chemical insecticides, including 

systemic products, in forests and natural areas. 

Options for managing EAB in forests may 

someday include microbial insecticides or perhaps 

entomopathogenic products. In the United States and 

many other countries, populations of foliar feeding 

Lepidoptera are commonly suppressed (or even 

eradicated) with aerial applications of Bt products 

(Bacillus thuringiensis var. kurstaki) (Tobin and 

Blackburn, 2007; Hajek and Tobin, 2011; Suckling et 

al., 2012; Tobin et al., 2014). However, there are as yet 

no effective microbial insecticides for EAB that can 

be applied in forested settings or across large areas. 

Researchers from federal agencies, along with private 

companies, continue to investigate Bt strains that 

could potentially be used to control adult EAB beetles 

(Bauer et al., 2012). Aerial applications of Spinosad 

(Saccharopolyspora spinosa Mertz and Yao) in woodlots 

with EAB infestations have been evaluated on a trial 

basis (Lewis and Smitley, 2012). Spinosad is a microbial 
CHAPTER 4: OTHER OPTIONS FOR EAB MANAGEMENT: ERADICATION AND CHEMICAL CONTROL

79 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

product that affects a broad range of plant-feeding 

insects, but may be less likely to harm predatory 

insects or parasitoids. Other research has focused 

on entomopathogens, such as the generalist fungal 

pathogen Beauveria bassiana (Bals.-Criv.) Vuill., and 

efficient methods to infect EAB or enhance efficacy 

or persistence of these products (Liu and Bauer, 2006; 

Lyons et al., 2012). 

Bioinsecticides could eventually play a role in 

integrated management programs for EAB in forests, if 

they can be economically produced, effectively applied, 

and can suppress EAB without harming a wide range 

of other invertebrates. Life history traits, however, 

suggest EAB may be less amenable to control via aerial 

application of Bt or related products than Lepidopteran 

forest pests like gypsy moth (Lymantria dispar L). 

Individual EAB adults have a relatively long life span 

and in a given area, adult EAB may be active for at least 

10 to 12 weeks during the summer. In addition, EAB 

adults, particularly mature females, spend considerable 

time on branches or the trunk. Aerially applied 

products will likely, therefore, need to penetrate the 

canopy of overstory trees, which can be challenging 

during the summer. Whether aerially applied microbial 

insecticides can persist long enough and reach foliage 

where most adult EAB are feeding under operational 

conditions remains to be determined. Given these 

problems, effective biological control of EAB, whether 

by native natural enemies or introduced parasitoids, 

may be critical for preventing the functional loss of 

many ash species in forest ecosystems across North 

America (Burr and McCullough, 2014; Klooster et al., 

2014; Knight et al., 2013). 

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Chapter 5: history oF emerald ash Borer BiologiCal Control 

Juli R. Gould1, Leah S. Bauer2, Jian J. Duan3, David Williams1, and Houping Liu4 

1

USDA APHIS PPQ, Center for Plant Health Science and Technology, Buzzards Bay, Massachusetts 02542
 

2

USDA Forest Service, Northern Research Station, East Lansing, Michigan 48823
 

3

USDA ARS, Beneficial Insects Introduction Research Unit, Newark, Delaware 19713
 

4

Pennsylvania Department of Conservation and Natural Resources, Bureau of Forestry, Harrisburg, Pennsylvania 17105
 

introdUCtion 

The search for natural enemies of the emerald 

ash borer (EAB), Agrilus planipennis Fairmaire 

(Coleoptera: Buprestidae), in northeastern Asia, 

its native range, was initiated within a year of its 

discovery in the United States (Bauer et al., 2005, 

2014). Although the official response to EAB’s 

invasion in both the United States and Canada was 

to regulate and attempt to eradicate EAB, the size 

and complexity of the outbreak prompted scientists 

and policy makers to support exploration for 

natural enemies as a potential tool for management 

of EAB. In 2008, when populations of EAB were 

already known to occur in nine states, the U.S. 

government moved from a policy of eradication 

to one of management (USDA-APHIS, 2013). By 

this time, scientists had completed all the steps 

necessary to secure permits for field release of 

three EAB natural enemies (host range assessment 

and safety evaluations) from China, and the use of 

these parasitoids was incorporated into the EAB 

management plan. This chapter documents the 

considerable efforts that went into making this 

possible in just five years. 

eaB natUral enemies From the 

United states 

Before pursuing classical biological control, it is 

important to determine if locally present natural 

enemies are attacking and affecting populations of 

the pest in the invaded area. After the discovery of 

EAB in Michigan in 2002, studies were conducted in 

Michigan and Pennsylvania that found several larval 

parasitoids but no egg parasitoids (Bauer et al. 2004, 

2005; Duan et al. 2009, 2013a). Most of these larval 

parasitoids are associated with native species 

of Agrilus (Taylor et al., 2012). Parasitism rates 

measured soon after the discovery of EAB in the 

United States were low (<1% in Michigan and 5% in 

Pennsylvania) compared to rates seen in Asia (Liu et 

al., 2003, 2007; Yang et al., 2005; Duan et al., 2012a) 

and rates reported in the literature for native Agrilus 

spp. in the United States. This low level of natural 

enemy attack on EAB was clearly inadequate to 

suppress EAB populations. Entomopathogenic fungi 

caused about 2% mortality of EAB life stages under 

the bark (Bauer et al., 2004). Predaceous beetles and 

woodpeckers also attacked EAB, but not in sufficient 

numbers to significantly affect EAB densities (Bauer 

et al., 2004; Lindell et al., 2008; Duan et al., 2011; 

Jennings et al., 2013). The lack of natural enemies 

capable of suppressing EAB populations below a 

density permitting survival of native ash trees was of 

great importance (Federal Register, 2007), and this 

risk supported the decision to introduce parasitoids 

that coevolved with EAB in Asia for biological control 

of EAB in North America (Bauer et al., 2008). 

eXploration in asia For emerald 

ash Borer natUral enemies 

Natural Enemy Surveys in China 

Initially, exploration for EAB natural enemies focused 

on China (Liu et al., 2003), investigating 11 locations 

in six areas where EAB had previously been reported: 

the provinces of Heilongjiang, Jilin, Liaoning, Hebei, 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

and Shandong, as well as the city-province of Tianjin 

(Yu, 1992; Xu, 2003). EAB was found in all provinces 

except Shandong (Liu et al., 2003). By 2002, these 

surveys in China had identified two larval parasitoids 

of EAB, Spathius sp. (Hymenoptera: Braconidae) 

and Tetrastichus sp. (Hymenoptera: Eulophidae) (Liu 

et al., 2003), and later in 2004, one egg parasitoid, 

Oobius sp. (Hymeoptera: Encyrtidae) was found 

(Zhang et al., 2005). These species were later 

described as Spathius agrili Yang (Yang et al., 2005), 

Tetrastichus planipennisi Yang (Yang et al., 2006), and 

Oobius agrili Zhang and Huang (Zhang et al., 2005). 

In depth studies of the population dynamics 

of EAB and its natural enemies were carried out in 

Jilin and Liaoning Provinces in northeastern China 

in 2004 and 2005. The two most abundant natural 

enemies of EAB, collected from EAB-infested 

Fraxinus pennsylvanica Marshall (native to eastern 

North America) in Jilin Province, were the larval 

parasitoid T. planipennisi and the egg parasitoid O. 

agrili (Liu et al., 2007). During the course of this 

study, these two parasitoid species reduced EAB 

densities by an estimated 74% in the infested trees. 

Tetrastichus planipennisi is also known from other 

provinces in northeast China, including Hebei (LSB 

unpublished data) and Heilongjiang (Yang et al., 

2006). 

Tetrastichus planipennisi is a gregarious 

endoparasitoid that attacks EAB larvae by drilling 

through the tree bark with its ovipositor. Brood sizes 

(number of eggs laid per host larva) range from 4 to 

172 (Yang et al., 2006; Ulyshen et al., 2010). The EAB 

larva continues feeding as parasitoid larvae develop 

inside its body; eventually the parasitoids consume 

most of the EAB larva and emerge into the gallery, 

where they pupate and develop into adults. Adult 

wasps chew through the bark and emerge. There 

are up to four such generations per year. Average 

parasitism of larvae by T. planipennisi in China was 

22.4%, but reached up to 65% (Liu et al., 2003, 2007; 

Yang et al., 2006). 

Oobius agrili is a small (1 mm long), 

parthenogenic wasp that lays its eggs singly inside 

EAB eggs. In general, adults from the first generation 

emerge to attack more EAB eggs, while wasps of the 

second generation enter diapause and overwinter 

inside the host egg. However, some individuals of 

the first generation of O. agrili do not emerge until 

the following spring. Parasitism of EAB eggs was as 

high as 61.5% by the end of the field season at some 

locations in northeastern China (Liu et al., 2007).

 Although scarce in northeast China, S. agrili, 

the third EAB parasitoid from China, was most 

abundant in Tianjin City in planted stands of 

Fraxinus velutina Torr. (native to the southwestern 

North America) (Xu, 2003; Liu et al., 2003; Yang et 

al., 2005). Parasitism of EAB larvae by S. agrili was as 

high as 90% in some stands in Tianjin by the end of 

the season (Yang et al., 2010). Spathius agrili females 

use their ovipositor to drill through the bark into the 

EAB larva, inject venom to paralyze it, and lay an 

average of five eggs per host larva (Gould et al., 2011). 

The parasitoid larvae hatch and feed externally on the 

EAB larva. Mature parasitoids pupate inside cocoons 

in the gallery, and adult wasps chew through the bark 

to emerge. Yang et al. (2010) estimate that S. agrili 

completes 3-4 generations per year in Tianjin. 

A fourth species of parasitic wasp, in the genus 

Sclerodermus (Hymenoptera: Bethylidae), was 

discovered parasitizing mature EAB larvae and pupae 

in Tianjin (Wu et al., 2008) and later described as 

Sclerodermus pupariae Yang et Yao (Yang et al., 2012). 

After locating a host, female wasps chew through 

the bark and use their strong front legs to excavate a 

tunnel through the tightly packed EAB frass in the 

host gallery to locate host larvae or pupae. They then 

sting and paralyze their host, feed on the hemolymph, 

and lay an average of 40 eggs per host. After hatching, 

S. pupariae larvae feed externally on the host and, 

with some maternal care during the larval stage, 

pupate inside cocoons. Approximately 13% of the 

EAB sampled in Tianjin were parasitized by S. 

pupariae (Yang et al., 2012). 

Natural Enemy Surveys in the Russian Far East 

Exploration for EAB parasitoids in Russia was 

concentrated near Vladivostok and Khabarovsk, 

where EAB is native (Williams et al., 2010; Duan 

et al., 2012a). As in China, ash trees native to 

Asia (F. mandshurica Rupr. and F. chinesis Roxb. 

subsp. rhynchophylla) and to North America (F. 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

pennsylvanica) were sampled in both natural forests 

and urban areas. Little parasitism was noted in 

Khabarovsk, but three larval parasitoid species were 

recovered in the Vladivostok region (Duan et al., 

2012a), as well as a strain of egg parasitoid in the 

genus Oobius that completes one generation per year 

and, based on DNA evidence, appears to be a different 

species than O. agrili from China (JJD, unpublished 

data). The larval parasitoids, mainly attacking EAB in 

F. pennsylvanica, included T. planipennisi, Atanycolus 

nigriventris Vojnovskaja-Krieger, and a previously 

unknown species of Spathius. The latter species was 

recently described as Spathius galinae Belokobylskij, 

and although its general biology is similar to that 

of S. agrili, it has a longer ovipositor and may be 

better adapted to the cold climate of the north 

central United States (Belokobylskij et al., 2012). 

Depending on the site and year, parasitism rates were 

approximately 24% for T. planipennisi, 23% for A. 

nigriventris, 76% for S. galinae, and 28% for O. agrili 

(Duan et al. 2012a; JJD unpublished data). 

Natural Enemy Surveys in South Korea 

Emerald ash borer is quite rare in South Korea and 

is probably kept in check by a combination of host 

resistance and natural enemies (Williams et al., 

2010). After several years of exploration, two EAB 

populations were discovered attacking F. chinesis 

subsp. rhynchophylla and F. mandshurica. One EAB 

population was found in stressed landscape trees 

near the city of Daejeon, and the other was on trees 

damaged during construction further north at a 

site near Seoul. At these sites, three natural enemy 

species were discovered: a larval ectoparasitoid 

later identified as S. galinae, a larval endoparasitoid 

tentatively identified as Tetrastichus telon Graham, 

and the clerid beetle Teneroides maculicollis Lewis. 

The clerid attacked EAB in the overwintering pupal 

chamber, where it pupated after consuming the host. 

The three species were brought to a United States 

quarantine facility; however, colonies could not be 

established. 

Surveys for Natural Enemies in 

Mongolia/Japan 

Although A. planipennis has been reported from 

Japan (Schaefer, 2004) it is quite rare (Haack et al., 

2002). A Japanese buprestid specialist returned to a 

locality from which A. planipennis had previously 

been collected and found a single adult beetle on a 

leaf. In Fukui Prefecture, Honshu, Japan, EAB is listed 

as endangered because only two collection locations 

have been recorded. Natural enemies of EAB were not 

recovered in Japan (Schaefer, 2005). 

Foreign exploration in Mongolia was even more 

fruitless (Schaefer, 2005). Not only were no EAB 

populations found, but collectors could not even find 

ash trees. No species in the genus Fraxinus occur in 

the published list of Mongolian vascular plants, and 

A. planipennis has not been recorded from Mongolia. 

Schaefer (2005) hypothesized that someone may 

have erred and associated collection of EAB from 

Mongolia when the discovery may instead have been 

in Inner Mongolia, China, where EAB is thought to 

occur. 

seleCtion oF potential 

BiologiCal Control agents 

Just because a natural enemy is found attacking the 

target pest in its native range does not necessarily 

make it suitable for use as a biological control 

agent (González and Gilstrap, 1992). Sclerodermus 

pupariae has several features lowering its potential 

as a biological control agent: (1) many females lack 

wings and would not disperse well, (2) the percentage 

parasitism observed in China was low, (3) it had 

a broad host range, and (4) members of the genus 

are known to sting humans (Gordh and Maczar, 

1990; Tang et al., 2012; Yang et al., 2012; Wei et al., 

2013). Therefore, this species was not considered for 

importation as a potential biological control agent for 

EAB. In contrast, A. nigriventris has better potential 

for use against EAB; however, scientists have yet to 

succeed in getting them to mate in the laboratory 

(JJD personal communication). Host specificity 

testing would also need to be conducted carefully 
CHAPTER 5: HISTORY OF EMERALD ASH BORER BIOLOGICAL CONTROL

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

because Atanycolus species native to the United States 

tend to have a broad host range and are known to 

attack EAB, often in large numbers (Cappaert and 

McCullough, 2009). 

Oobius agrili, T. planipennisi, S. agrili, and S. 

galinae were all considered promising candidates 

for biological control. All four species possess 

characteristics considered by Kimberling (2004) as 

enhancing the likelihood of successful biocontrol: 

female-biased sex ratio or parthenogenesis, a short 

generation time, and high rates of parasitism and 

fecundity. These four species were imported into 

quarantine in the United States for host range testing. 

Quarantine Screening 

Rearing EAB and its parasitoids. Before 

scientists could study the biology and host 

preferences of EAB parasitoids, it was necessary 

to develop methods to rear both EAB and the 

parasitoids (see Ch. 8). There were several challenges 

that needed to be met: (1) parasitoids can potentially 

be reared all year but EAB is univoltine and has an 

obligatory diapause as mature larvae, (2) adult EAB 

eat ash leaves, but leaves are only available in the 

field in the summer, (3) EAB eggs are needed for 

rearing the egg parasitoid O. agrili, and (4) the larval 

parasitoids only attack EAB when it is beneath ash 

bark. 

The dilemma of EAB availability was solved by 

felling ash trees containing large numbers of EAB 

and storing the logs in cold rooms until the insects 

were needed. Felling of ash trees could be done (1) 

during the late summer when logs contained mature 

larvae appropriate for rearing larval parasitoids or (2) 

during the winter when overwintering mature fourthinstar larvae were present in their pupation cells (as 

J-larvae), which quickly developed into EAB adults 

when warmed. 

The need to obtain foliage to feed adults 

throughout the year was solved by rearing tropical 

or Shamel ash, Fraxinus uhdei (Wenz.) Lingelsh., in 

greenhouses. 

Initially, small ash logs wrapped in curling ribbon 

were presented to adult beetles for oviposition, but a 

method of coaxing females to lay eggs on coffee filters 

was later developed. Eggs on filter papers could then 

be presented to O. agrili for parasitization. 

EAB larvae were extracted from the logs by 

peeling the bark, and these larvae were reinserted 

in grooves under bark flaps of small ash logs for 

presentation to S. agrili and T. planipennisi (Gould et 

al., 2011). This method was laborious and was later 

improved upon for mass production (see Ch. 8). 

Host specificity testing. Biological control of 

insect pests using entomophagous natural enemies 

has generally been considered “natural” and “safe.” 

However recent studies have documented negative 

impacts on non-target species in some cases 

(Boettner et al., 2000; Obrycki et al., 2000; Henneman 

and Marmot, 2001), highlighting the need for prerelease host specificity testing. The specificity of 

EAB parasitoids imported from China or Russia 

was estimated in quarantine as part of the process of 

assembling data needed to apply for release permits. 

Specificity of agents is summarized below. 

(1) Spathius agrili. No-choice host specificity 

tests with S. agrili were conducted in China and the 

United States to determine possible direct effects 

on non-target species (Yang et al., 2008). Spathius 

agrili finds hosts to parasitize by hearing sounds or 

feeling vibrations produced by feeding larvae inside 

wood. All test larvae, therefore, were presented while 

feeding inside their natural host trees. In initial nochoice host specificity tests, S. agrili did not parasitize 

wood-boring Lepidoptera, a longhorned beetle 

(Cerambycidae), or the one Agrilus species tested. Of 

these three species (whose larvae all attack ash), only 

EAB was parasitized. Further testing was, therefore, 

confined to members of the genus Agrilus, which 

were hypothesized to potentially be at risk because 

they were closely related to EAB. 

In the United States, we tested the two-lined 

chestnut borer, Agrilus bilineatus Weber, in oak 

(Quercus), and the bronze birch borer, Agrilus anxius 

Gory, in birch (Betula), while in China various other 

local Agrilus species were tested. 

In no-choice tests, S. agrili attacked some species 

of Agrilus other than EAB, but at rates that were 

significantly lower than for emerald ash borer. In 

China, S. agrili attacked Agrilus zanthoxylumi Hou, 

Agrilus mali Matsumura, and Agrilus inamoenus 

Kerremans. No attack occurred on other Agrilus 
CHAPTER 5: HISTORY OF EMERALD ASH BORER BIOLOGICAL CONTROL

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

species tested, Sphenoptera sp. (Coleoptera: 

Buprestidae), or Eucryptorrhynchus chinensis (Olivier) 

(Coleoptera: Curculionidae) (Yang et al., 2008). 

No-choice tests determine the physiological host 

range of a parasitoid by giving them no other option 

but to oviposit on a non-target host. Parasitoid adult 

orientation to host plants is not part of the test and so 

this filter is disregarded. To determine the ecological 

host range of S. agrili, olfactometer tests with adults 

were conducted in China to determine if S. agrili 

were attracted to the plant species harboring the 

larvae tested in no-choice tests. Naïve, mated S. agrili 

females were placed in vertical y-tube olfactometers 

and given a choice of leaves and twigs of various host 

plants or clean air. Spathius agrili was only attracted to 

two ash species (F. pennsylvanica and F. velutina) and 

one species of willow (Salix babylonica L.) (Yang et al., 

2008). Even though some attack occurred on larvae 

found in Citrus reticulata Blanco, Malus micromalus 

Makino, and Zanthoxylum bungeanum Maxim in 

no-choice tests, S. agrili females were not attracted 

to these tree species. In nature, if parasitoids are not 

attracted to an insect’s host tree, they would be unlikely 

to encounter and parasitize larvae of that non-target 

species. Spathius agrili was attracted to willow leaves, 

and at least three Agrilus species attack willow in the 

United States: Agrilus pratensis pratensis Ratzburg 

(adults 4 - 6 mm long), Agrilus politus Say (adults 

5.0 - 8.5 mm long), and Agrilus quadriguttatus Gory. 

These insects are quite small compared with adult EAB, 

which are 8.5-13.5 mm long. Spathius agrili attacks 

only large EAB larvae, and even mature larvae of A. 

pratensis and A. politus are likely too small to be at risk 

of attack. Thus even if S. agrili is attracted to willow in 

the United States, it is unlikely to encounter any nontarget species large enough to be suitable hosts. 

Another piece of evidence concerning host 

specificity was gathered in China by collecting larvae 

of six Agrilus species in the field and then rearing them 

to determine their parasitoid fauna. A total of 2,074 

Agrilus larvae of six non-target species were collected 

and neither S. agrili nor T. planipennisi were recovered 

(Yang et al., 2008). Given the combination of evidence 

from no-choice tests (lower parasitism rates or no 

attack on non-target Agrilus species), olfactometer 

tests (only attracted to ash and willow), and the lack of 

S. agrili reared from other Agrilus species in China, it 

was predicted that release of S. agrili would not have 

adverse direct effects on non-target species in the 

United States. 

(2) Tetrastichus planipennisi. To evaluate the 

direct effects of T. planipennisi on potential non-target 

North American insect species, no-choice assays were 

performed in the laboratory with larvae of EAB and 

eight species of buprestids (five species of Agrilus 

and three of Chrysobothris), five cerambycids, two 

lepidopterans, and one hymenopteran (Liu and Bauer, 

2007; Federal Register, 2007). These insects were 

selected based on (1) the degree of taxonomic closeness 

to EAB; (2) overlap in habitat and/or niche with EAB; 

(3) risk to beneficial, threatened, or endangered insects; 

and (4) feasibility of acquiring or rearing enough larvae 

to perform replicated assays. Tetrastichus planipennisi 

did not attack any of the seventeen non-target species 

presented in no-choice tests, it was considered quite 

host specific, and further testing was not done. 

(3) Oobius agrili. To evaluate the direct effects 

of O. agrili on non-target insect species, no-choice 

assays were performed in the laboratory using eggs 

of six Agrilus species, two cerambycids, and four 

lepidopterans (Bauer and Liu, 2007; Federal Register, 

2007). In no-choice assays, O. agrili did not oviposit in 

eggs of the cerambycids or lepidoptera. Oobius agrili 

may oviposit and develop in Agrilus eggs from different 

species if they have eggs similar in size to those of 

EAB. Such non-target species include A. anxius 

(bronze birch borer), A. bilineatus (two-lined chestnut 

borer), and Agrilus ruficollis (F.) (red-necked cane 

borer), which are pests of birch, oak, and raspberry, 

respectively. Paired no-choice and choice assays were 

then performed for two of the Agrilus species that 

were accepted by O. agrili during the no-choice assays. 

In the choice assays, O. agrili preferred eggs of A. 

planipennis (EAB) on ash logs over those of A. anxius 

or A. ruficollis, on birch and raspberry, respectively. 

(4) Spathius galinae. To evaluate the effects of 

S. galinae on non-target insect species, no-choice and 

choice host specificity tests were conducted (JRG and 

JJD unpublished). Fifteen North American species 

of wood-boring insects were exposed to S. galinae 

to assess the parasitoid’s physiological host range. 

Emphasis was placed on species closely related to the 
CHAPTER 5: HISTORY OF EMERALD ASH BORER BIOLOGICAL CONTROL

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

target pest or those feeding on ash. Thirteen of these 

fifteen species were wood-boring beetles, one was 

a clearwing moth (Lepidoptera: Sesiidae) and one 

a sawfly (Hymenoptera: Cephidae). Of the beetles, 

five were in the genus Agrilus, and were thus closely 

related to the EAB, and another was in the same 

family (Buprestidae). Three of the insects tested – the 

longhorned beetle Neoclytus acuminatus (F.), the clearwinged moth (Podosesia sp.), and the eastern ash bark 

beetle, Hylesinus fraxini Panz. (Coleop.: Scolytinae) – 

attack ash as their main host and would be susceptible 

to parasitism if S. galinae accepts any boring insects 

infesting ash. 

Spathius galinae attacked only one species other 

than the EAB, the gold spotted oak borer (Agrilus 

auroguttatus Schaeffer) in red oak (Quercus rubra L.). 

This species is an invasive borer killing native oaks in 

California. The rate of parasitism was, however, lower 

(only 41%) on the non-target host compared to EAB 

(71%) under test conditions that strongly favored 

parasitism. Spathius galinae did not attack the other 

three test species that infested red oak, nor did it attack 

the other Agrilus or the three non-Agrilus species 

infesting ash. This level of host specificity is quite 

high; indeed, higher than that of S. agrili, which was 

approved for release against EAB. 

Applying for Release Permits 

Applying for permits to release exotic parasitoids 

against invasive pests in the United States is a 

complicated process involving review by the North 

American Plant Protection Organization (NAPPO), 

whose members include the United States, Canada, and 

Mexico, by the U.S Fish and Wildlife Service, North 

American Indian Tribes, the USDA-APHIS permitting 

unit, and State Departments of Agriculture (Bauer et 

al., 2014). The application must also be posted in the 

Federal Register for public comment before APHIS 

approves or disapproves the application. In January, 

2007, USDA scientists applied for environmental 

release permits for S. agrili, T. planipennisi, and O. 

agrili in Michigan. The permits were granted at the 

end of July 2007, and the parasitoid species were 

released at several sites in Michigan. The application to 

release S. galinae was submitted in March, 2013 and in 

November of that year was approved by the NAPPO 

committee. The final outcome of the permit application 

to release S. galinae in the United States was pending in 

January 2015. 

Field estaBlishment and 

evalUation oF natUral enemies 

Rearing and Release 

After release permits were issued in 2007, relatively 

small numbers of adult S. agrili, T. planipennisi, and 

O. agrili were released at field sites in Michigan. 

Releases were expanded to new sites in Ohio and 

Indiana in 2008, and to Illinois and Maryland in 

2009, but only a few hundred adults of each species 

were released because of the limited rearing capacity 

of the USDA research laboratories. Despite these 

limitations, however, establishment of the three 

species was confirmed within two years at many 

of these field sites (Bauer et al., 2008, 2011). These 

early successes resulted in the decision by USDA to 

initiate an EAB Biological Control Program in 2009 

and construct the APHIS EAB Biocontrol Facility 

in Brighton, Michigan (USDA, 2013). Researchers 

wrote guidelines to assist land managers with basic 

information on EAB, the biological control agents, 

site selection, and methods for release and recovery 

of the parasitoids (Gould et al., 2013). An online 

database was also developed where the Guidelines 

are posted and parasitoids release and recovery 

data are entered and mapped (mapbiocontrol.org). 

The EAB biological control agents are now massreared for distribution and release throughout the 

still expanding EAB infestation in North America, 

and production and release methods continue to be 

improved (see Ch. 8). 

In 2009, the APHIS EAB Biocontrol Facility 

concentrated on rearing S. agrili, and 10,000 adult 

females of that species were reared and released (Fig. 

1) (J. Lelito, personal communication). In 2010, a 

concerted effort was made to increase production 

of T. planipennisi (Fig. 2), and production of the egg 

parasitoid, O. agrili, was greatly increased in 2011 

(Fig. 3). Production of these parasitoids increased 
CHAPTER 5: HISTORY OF EMERALD ASH BORER BIOLOGICAL CONTROL

BIOLOGY AND CONTROL OF EMERALD ASH BORER

0 

10 

20 

30 

40 

50 

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0 

10000 

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50000 

60000 

70000 

80000 

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100000 

2007 2008 2009 2010 2011 2012 2013 

Number of Release Sites 

Number of Females 

Year 

Number of Females Released 

Number of Release Sites 

Figure 1. Number of female Spathius 

agrili released against emerald ash 

borer 2007-2013 and the number of 

release sites in the United States. 

0 

50,000 

100,000 

150,000 

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250,000 

300,000 

350,000 

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Number of Females 

Number of Females Released 

Number of Release Sites 

100
 

90
 

80
 

70
 

Figure 2. Number of female 

60
 Tetrastichus planipennisi released 

against emerald ash borer 2007­ 50
 2013 and the number of release 

sites in the United States. 40
 

30
 

20
 

10
 

0
 

2007 2008 2009 2010 2011 2012 2013
 

Year 

0 

10 

20 

30 

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0 

10,000 

20,000 

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70,000 

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90,000 

100,000 

2007 2008 2009 2010 2011 2012 2013 

Number of Release Sites 

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Number of Females Released 

Number of Release Sites 

Figure 3. Number of female Oobius 


agrili released against emerald ash 


borer 2007- 2013 and the number of 


release sites in the United States.
 

Number of Release Sites 

89 
CHAPTER 5: HISTORY OF EMERALD ASH BORER BIOLOGICAL CONTROL

90 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

in subsequent years, with the exception of S. agrili, 

which was not released in northern states after 2012 

(see the Establishment section for explanation). The 

increased production was necessary because each 

year at least two more states initiated releases of 

EAB parasitoids (Table 1), so that by 2013 seventeen 

states were conducting releases. In 2014 Colorado, 

Georgia, New Hampshire, and New Jersey discovered 

populations of EAB and releases in those states were 

set to begin that year. 

To improve parasitoid production and release 

efficiency, the APHIS EAB Biocontrol Facility began 

modifying the shipment and release methods for the 

three EAB biological control agents. Before 2012, 

parasitoids were released as adults. This was done 

by rearing them to the adult stage in the laboratory, 

consolidating them into plastic cups provisioned 

with honey, and shipping them inside coolers to 

cooperators who released them onto the trunks 

of EAB-infested ash trees. In 2012, APHIS began 

shipping parasitoids as mature larvae or pupae for 

self-emergence in the field from cups containing 

parasitized EAB eggs for O. agrili or ash bolts 

containing EAB larvae parasitized with either T. 

planipennisi or S. agrili. This change began for O. 

agrili in 2012 and for the two larval parasitoid species 

in 2013. Further research is needed to evaluate the 

success of the newer release methods. 

Establishment 

Sampling methods. Sampling EAB to determine 

whether or not larvae or eggs are parasitized poses 

quite a challenge. EAB eggs are small and laid 

between layers of bark and in bark crevices. EAB 

larvae feed beneath the bark of ash trees, and to 

recover them the bark must be peeled off to expose 

the larvae. If the goal is to determine the percentage 

of EAB that are parasitized, one must search ash trees 

for EAB eggs and larvae. 

However, if the goal is only to confirm 

establishment, several additional methods have been 

developed (Bauer et al., 2012; Duan et al., 2011, 

2012b). For detection of O. agrili, laboratory-reared 

EAB eggs can be placed in the field under bark flaps, 

on small ash logs, or in cups on paper. For the larval 

parasitoids, EAB larvae can be inserted in small ash 

Table 1. States initiating releases of EAB parasitoids 

by year. 

Year States Inititiating Releases 

2007 Michigan 

2008 Ohio, Indiana 

2009 Illinois, Maryland 

West Virginia, Kentucky, New York, 2010 

Wisconsin 

2011 Pennsylvania, Minnesota, Virginia 

2012 Missouri. Tennessee 

Massachusetts, North Carolina, 

2013 

Connecticut 

logs and placed in the field. Creating these “sentinel” 

eggs or larvae, however, requires either rearing adult 

EAB or collecting larvae for insertion in the sentinel 

logs. EAB parasitoids have been recovered at several 

sites using sentinel logs, and egg sentinel logs were 

used to document the phenology of O. agrili activity 

in the field in Michigan (Abell et al., 2011). 

Both larval and egg parasitoids can also be 

recovered by collecting logs or bark samples and 

placing them in cardboard rearing tubes fitted with 

collection jars. The emerging parasitoid adults are 

attracted to the light in the jar and essentially collect 

themselves. 

Finally, adult parasitoids can be recovered in 

the field using yellow pan traps filled with a solution 

of propylene glycol (Bauer et al., 2013). These traps 

are inexpensive to produce and easy to deploy, but 

distinguishing the biological control agents from 

similar native species requires individuals trained in 

insect taxonomy and identification. 

Pheromones have been identified for both S. 

agrili and T. planipennisi (Bauer et al., 2011; Cossé et 

al., 2012), and the use of pheromone lures is being 

investigated as a method to increase the efficacy of 

yellow pan traps. 

Reproduction, overwintering, and establishment. 

For the introduced parasitoids to successfully 
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control EAB, they must find conditions suitable 

for reproduction in the field, survive cold winter 

temperatures, and persist from year to year. The three 

introduced parasitoids released as EAB biological 

control agents have several generations per year, 

and their presence in the field must coincide with 

the availability of the stages suitable for parasitism 

(eggs for O. agrili and larvae for S. agrili and T. 

planipennisi). Throughout their adult lives, the 

parasitoid must also find sources of nourishment such 

as nectar or honeydew. 

Spathius agrili was found parasitizing 18% of 

the EAB larvae sampled the spring following the 

release of 175 females in 2007 in southern MI (JRG 

unpublished). However, samples collected from 40 

ash trees the following year revealed not a single 

parasitoid. At another site, parasitism one year 

after release was 45%. Two broods were discovered 

each of the following two years, but parasitism by 

S. agrili remained consistently low. At six more 

intensively sampled study sites in Michigan, S. agrili 

was recovered in yellow pan traps, but only two EAB 

larvae parasitized by this species were recovered 

after 2-5 years of sampling (Duan et al., 2013b). 

Spathius agrili also does not seem to have persisted 

in Maryland or Ohio. One possible explanation for 

this apparent lack of persistence is that the population 

of S. agrili reared for release in the United States 

originated from Tianjin, China. The latitude of this 

city is near the 39th parallel, and the climate there is 

a better match for the central (north-south) rather 

than the northern United States. Spathius agrili can 

successfully overwinter in the midwestern United 

States, so cold is probably not the limiting factor. 

Perhaps there is a problem with synchrony between 

the emergence of adult S. agrili and availability of the 

mature EAB larvae that they need to attack. Based 

on this observation, the EAB Biocontrol Program 

decided in 2013 to cease releasing S. agrili above 

the 40th parallel in North America. If S. galinae 

is approved for release, we anticipate that it will 

be better synchronized with its EAB host in the 

more northern states. Spathius agrili has also been 

recovered in Illinois, Indiana, Pennsylvania, New 

York and Tennessee, and we are especially interested 

in whether S. agrili will persist in Tennessee, where 

the climate is more similar to the parasitoid’s native 

range in China. 

Oobius agrili has been recovered in Michigan, 

Ohio, Indiana, Pennsylvania, Maryland, and New 

York. At two sites in Michigan, parasitism by O. agrili 

increased from 5% one year following release to 20% 

two years later (Duan et al., 2011, 2012b; Abell et al., 

2011). This species was also recovered at non-release 

locations at least 800 m from the release site two years 

after release. Parasitized eggs were found on 73% of 

trees in the release plots and 25% of the trees in the 

control plots (Abell et al., 2014), providing evidence 

that O. agrili populations are slowly building and 

dispersing in Michigan. 

Establishment and spread of T. planipennisi is 

even more impressive. At six intensively studied 

sites in Michigan, 92% of the trees at the release 

sites contained at least one brood of T. planipennisi 

four years after release, and parasitism levels 

increased steadily to an average of over 20% (Duan 

et al., 2013b). Parasitism by T. planipennisi at the 

six control sites (at least 1 km away) also increased 

yearly to an average level of 13% after four years. The 

rearing facility in Brighton, Michigan, often finds T. 

planipennisi in trees harvested far from known release 

locations. It is not known whether T. planipennisi is 

dispersing so well on its own or by human movement 

of infested firewood, or both. Tetrastichus planipennisi 

has also been recovered from Illinois, Indiana, Ohio, 

New York, Maryland, Wisconsin, and Minnesota. 

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97 

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Chapter 6: Biology oF emerald ash Borer parasitoids 

Leah S. Bauer,1 Jian J. Duan,2 Jonathan P. Lelito,3 Houping Liu,4 and Juli R. Gould5 

1

USDA Forest Service, Northern Research Station, Lansing, Michigan 48910
 

2

USDA ARS, Beneficial Insects Introduction Research Unit, Newark, Delaware 19713
 

3

USDA APHIS, Plant Protection and Quarantine, Brighton, Michigan 48116
 

4

Pennsylvania Department of Conservation and Natural Resources, Bureau of Forestry, Harrisburg, Pennsylvania 17105
 

5

USDA APHIS, Center for Plant Health Science and Technology, Buzzards Bay, Massachusetts 02542
 

introdUCtion 

The emerald ash borer (EAB) (Agrilus planipennis 

Fairmaire (Coleoptera: Buprestidae), an invasive 

beetle introduced from China (Bray et al., 2011), was 

identified as the cause of ash (Fraxinus spp.) mortality 

in southeast Michigan and nearby Ontario in 2002 

(Haack et al., 2002; Federal Register, 2003; Cappaert 

et al., 2005). Although eradication was attempted for 

several years after the beetle’s discovery, it continued 

to spread throughout North America, killing ash trees 

in urban, forested, and riparian areas. In an effort 

to conserve native species of Fraxinus, researchers 

continue to evaluate integrated pest management 

methods that include the use of classical biological 

control, systemic insecticides, and the development of 

resistant cultivars (Herms and McCullough, 2014). 

Surveys of EAB populations in recently invaded 

areas of North America revealed a low prevalence 

of native generalist parasitoids, mainly species in 

Atanycolus and Spathius (Hymenop.: Braconidae), 

and Phasgonophora sulcata Westwood (Hymenop.: 

Chalcididae) (Bauer et al., 2004; Lindell et al., 2008; 

Duan et al., 2009, 2012a, 2013a). In regions of China 

where EAB is native, specialist EAB parasitoids were 

recovered (Liu, H-Q. et al., 1996; Liu, H-P. et al., 2003, 

2007; Zhang et al., 2005; Yang et al., 2005). The most 

promising of these parasitoids for EAB biocontrol in 

North America were Oobius agrili Zhang and Huang 

(Hymenop.: Encyrtidae), Tetrastichus planipennisi Yang 

(Eulophidae), and Spathius agrili Yang (Hymenop.: 

Braconidae). 

Following research on the biology, host specificity, 

and impacts of these parasitoid species on EAB 

population dynamics in China, researchers 

proposed their release as EAB biocontrol agents in 

the continental United States in an Environmental 

Assessment (Federal Register, 2007). After a public 

comment period in 2007, regulatory agencies 

involved in biological control risk-benefit analyses 

approved trial releases of the three parasitoid species 

in Michigan, permits were issued, and releases began 

(Bauer et al., 2008, 2009, 2014, in press). Establishment 

of the introduced parasitoids was confirmed within 

a year of their first release, leading to the decision 

by USDA to initiate the EAB Biocontrol Program, 

construction of an EAB-parasitoid rearing facility in 

Brighton, Michigan, and development of an online 

database where parasitoids can be requested and 

data on parasitoid releases, recoveries, and mapping 

are stored (USDA FS, 2009; Bauer et al., 2010ab; 

MapBioControl, 2014). As a result, EAB biological 

control agents are being released in other states with 

known EAB infestations. In addition, another larval 

parasitoid of EAB from the Russian Far East, Spathius 

galinae Belokobylskij (Hymenop.: Braconidae), is being 

considered for release in the future (Belokobylskij et al., 

2012; Duan et al., 2012b). 

To improve the integrated pest management of 

EAB in forest ecosystems using classical biological 

control, researchers have been studying the introduced 

and native natural enemies of EAB populations at longterm study sites in Michigan and other states (Bauer 

et al., in press; Duan et al., 2010, 2012a, 2013b, 2014a; 

Jennings et al., 2014). In this chapter, we will review the 

literature on the biology of key parasitoids known to 

attack EAB in North America and Asia. 
CHAPTER 6: BIOLOGY OF EMERALD ASH BORER PARASITOIDS

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

Biology oF native or selFintrodUCed parasitoids 

attaCKing eaB in north ameriCa 

Several native parasitoids and one self-introduced 

exotic species are known to attack EAB larvae at field 

sites in North America; no native EAB egg parasitoids 

are known (Table 1). In general, the EAB larval 

parasitoids reported in North America are parasitoids 

of Agrilus spp., although several species also parasitize 

the larvae of other groups of wood-boring insects 

(Gibson, 2005; Duan et al., 2009; Taylor et al., 

2012). Rates of larval parasitism by these species are 

generally low (<5%) during the initial phase of the 

EAB invasion; however, there are reports in Michigan 

of increasing larval parasitism by parasitoids of other 

coleopteran woodborers (Cappaert and McCullough, 

2009; Duan et al., 2012a, 2014a). 

The most prevalent native parasitoids of EAB 

are several braconids in the genus Atanycolus and 

Table 1. List of reported hymenopteran parasitoids attacking emerald ash borer larvae or eggs. 

Name Family Parasitoid biology Reported Range 

Sclerodermus pupariae Bethylidae gregarious larval ectoparasitoid China 

Atanycolus cappaerti Braconidae solitary larval ectoparasitoid Michigan 

Atanycolus disputabilis ʺ ʺ Northeastern North America 

Atanycolus hicoriae ʺ ʺ Northeastern North America 

Atanycolus nigropopyga ʺ ʺ Northeastern North America 

Atanycolus nigriventris ʺ ʺ Russian Far East 

Atanycolus simplex ʺ ʺ Northeastern North America 

Spathius agrili1 ʺ gregarious larval ectoparasitoid China, Northeastern US 

Spathius floridanus2 (= Spathius

simillimus)

2 

ʺ ʺ Northeastern North America 

Spathius galinae3 ʺ ʺ Russian Far East, South Korea 

Spathius laflammei (= Spathius

benefactor ) 

ʺ ʺ United States 

Spathius polonicus ʺ ʺ Europe, Moscow 

Leluthia astigmata ʺ solitary larval endoparasitoid United States 

Phasgonophora sulcata Chalcididae solitary larval endoparasitoid Northeastern North America 

Oobius agrili1 Encyrtidae solitary parthenogenic egg parasitoid China, United States 

Oobius sp. ʺ ʺ Russian Far East 

Oencyrtus sp. ʺ solitary egg parasitoid China 

Tetrastichus planipennisi1,4 Eulophidae gregarious larval endoparasitoid China, Russian Far East, 

North America 

Tetrastichus sp. ʺ ʺ South Korea 

Balcha indica Eupelmidae solitary parthenogenic, larval 

ectoparasitoid 

Southeast Asia, Northeast- ern United States 

Eupelmus sp. ʺ solitary ectoparasitoid Northeastern North America 

Cubocephalus sp. Ichneumonidae solitary larval ectoparasitoid Northeastern North America 

Dolichomitus sp. ʺ ʺ Northeastern North America 

Orthizema sp. ʺ ʺ Northeastern North America 

1

 introduced as EAB biological control agents in the United States starting in 2007 

2

 recent evidence suggests these are separate species (JPL, J. Strazanac, N. Havill, unpublished data) 

3

 in 2015, proposed for release as an EAB biological control agent in the United States 

4 introduced as EAB biological control agent in Canada starting in 2013 

98 
CHAPTER 6: BIOLOGY OF EMERALD ASH BORER PARASITOIDS

99 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

the chalcidid Phasgonophora sulcata Westwood 

(Bauer et al., 2008; Duan et al., 2009, 2013a, 2014a). 

In the genus Atanycolus, A. cappaerti Marsh and 

Strazanac and A. hicoriae Shenefelt are the most 

common species found attacking EAB in Michigan, 

Ohio, or Pennsylvania, but A. simplex Cresson, A. 

nigropopyga Shenefelt, and A. disputabilis (Cresson) 

are also reported (Bauer et al., 2008; Cappaert and 

McCullough, 2009; Duan et al., 2013a). Other less 

common parasitoids include (1) several braconid 

species – Spathius floridanus Ashmead, S. simillimus 

Ashmead (see taxonomic changes below in section on 

Spathius biology), S. laflammei (= Spathius benefactor 

Matthews), and Leluthia astigmata (Ashmead); (2) 

several unknown ichneumonids in Dolichomitus, 

Orthizema, and Cubocephalus; and (3) two eupelmids 

– Eupelmus sp. and Balcha indica (Mani & Kaul) 

(Bauer et al., 2005, 2008; Duan et al., 2009, 2013a, 

2014a; Kula et al., 2010). These parasitoids are native 

except for B. indica, which is from Southeast Asia and 

is self-naturalized in the eastern United States where 

it attacks a range of wood-boring beetles (Gibson, 

2005). 

Atanycolus spp. (Braconidae) 

Marsh et al. (2009) reports 11 native species of 

Atanycolus in North America, which parasitize the 

larvae of Agrilus species or those of other woodboring beetles. The five Atanycolus species reported 

from species of Agrilus (Taylor et al., 2012) are 

solitary, ectoparasitic idiobionts of late-stage larvae 

that complete one or two generations in northern 

regions of the United States (Fig. 1a-d). Many of 

the Atanycolus adults reared in the laboratory from 

a b

c d

Figure 1. Atanycolus species life stages. (a) Atanycolus adult ovipositing onto an EAB larva in the trunk of an ash tree. (Photo credit: 

Houping Liu); (b) Atanycolus egg on an EAB larva photographed though a dissecting microscope (45X). (Photo credit: Deborah 

Miller); (c) Atanycolus larva feeding on an EAB larva in its gallery. (Photo credit: Deborah Miller); (d) Atanycolus cocoon containing a 

pupa with the remnant of its EAB larval host (to the left of the cocoon) in an EAB gallery. (Photo credit: David Cappaert) 
CHAPTER 6: BIOLOGY OF EMERALD ASH BORER PARASITOIDS

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

EAB larvae are relatively large wasps (5-7 mm long) 

with long ovipositors (4-6 mm) (Marsh et al., 2009). 

Consequently, they can parasitize EAB larvae in 

mature ash trees (>57 cm diameter at breast height 

[DBH]) with thick outer bark (up to 9 mm thick) 

(Abell et al., 2012). The biology of A. cappaerti, a 

recently described species found parasitizing EAB 

in Michigan, is best known and is typical of other 

Atanycolus species (Cappaert and McCullough, 2009; 

Marsh et al., 2009). 

The biology of A. cappaerti is reported from a 

field study in southern Michigan in 2007 and 2008 

(Cappaert and McCullough, 2009; Tluczek et al. 

2010). The life cycle of A. cappaerti is generally well 

synchronized with EAB in Michigan, with increasing 

numbers of cocoons found throughout the summer 

and fall from newly developing EAB larval hosts. 

By the end of October, A. cappaerti larvae are found 

parasitizing medium to large EAB larvae that are still 

actively feeding in the phloem. Atanycolus cappaerti 

also parasitizes the larvae of Agrilus liragus Barter & 

Brown and Agrilus bilineatus (Weber), demonstrating 

at least a genus-level host range for this parasitoid in 

Michigan forests (Cappaert and McCullough 2009). 

Due to similarities in the morphology and biology 

of A. cappaerti and A. hicoriae, another parasitoid 

of EAB larvae in Michigan, these two species are 

combined as “Atanycolus spp.” for studies on EAB 

population dynamics (e.g., Duan et al., 2013a, 2014a). 

Species of Atanycolus (Fig. 1a-d) overwinter as 

mature larvae or prepupae inside cocoons spun in 

EAB galleries during the fall. Adult emergence begins 

in early June, and these adults parasitize overwintered 

EAB larvae. Most first generation Atanycolus larvae 

complete their development in about one month, 

with emergence occurring in early to mid-July. These 

wasps parasitize the current year’s EAB larvae. The 

longevity of female wasps held in the laboratory 

averaged 32 days (JJD, unpublished data). As reported 

for other braconid parasitoids of Agrilus, some first 

generation larvae may enter diapause, overwinter, and 

emerge as adults the following spring. 

Spathius spp. (Braconidae) 

Species of the genus Spathius are gregarious 

ectoparasitic idiobionts of various coleopteran 

families including Cerambycidae, Buprestidae, 

Scolytinae, Curculionidae, Bostrichidae, and 

Anobiidae (Marsh and Strazanac, 2009). In North 

America, several species of Spathius are found 

attacking late-instar EAB larvae (Bauer et al. 2004; 

Duan et al., 2009) (Table 1). 

Spathius floridanus (Fig. 2a,b) and S. 

simillimus are the most common Spathius species 

found attacking EAB in Michigan (Bauer et al., 2004), 

while S. laflammei is the common species in western 

Pennsylvania (Duan et al., 2009) (Table 1). Following 

the initial identifications of the two species attacking 

EAB in Michigan, Marsh and Strazanac (2009) 

merged these into S. floridanus. Current evidence, 

however, suggests that S. floridanus and S. simillimus 

are distinct species (JPL, J. Strazanac, N. Havill, 

unpublished data). Although published literature 

is lacking on the biology of these native Spathius, 

laboratory studies in Michigan found Spathius 

adults emerged in late spring and early summer, 

and completed one or two generations before fall 

temperatures induced diapause in the remaining 

larvae; when reared in the laboratory at 25-27 oC, 

Spathius species completed a generation in 28-32 days 

(JPL, unpublished data). 

Phasgonophora sulcata (Chalcididae) 

Phasgonophora sulcata (Fig. 3a-d), native to eastern 

North America, is a solitary endoparasitic koinobiont 

of Agrilus larvae and completes one generation per 

year. It has been reared from A. anxius, A. bilineatus, 

A. liragus, and more recently from EAB in the United 

States and Canada (for review see Taylor et al., 2012). 

The emergence of P. sulcata adults lags about two 

weeks behind that of EAB adults (Roscoe, 2014). In 

the field in southern Michigan, these relatively large 

wasps (~8 mm long) are readily observed during late 

June through July seeking host larvae in EAB-infested 

ash trees. By sequential larval dissections throughout 

the season, we have observed the hatch and slow 

development of P. sulcata eggs and larvae in the 

posterior region of the host hemocoel. Preliminary 

studies suggest P. sulcata parasitizes first or second 

instar EAB larvae; pupation occurs the following 

spring inside host prepupae (LSB, unpublished data). 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

a b

Figure 2. Spathius floridanus life stages: (a) S. floridanus adult searching for EAB larvae in a small ash log in the
 

laboratory. (Photo credit: Jian Duan); (b) S. floridanus cocoons with pupae in an EAB larval gallery. (Photo credit: Jian Duan)
 

a b

c d

Figure 3. Phasgonophora sulcata life stages: (a) P. sulcata adult searching for EAB larva in a small ash log in the laboratory. (Photo 

credit: Deborah Miller); (b) P. sulcata egg dissected from a field-collected EAB larva. (Photo credit: Deborah Miller); (c) P. sulcata 

larva dissected from the posterior hemocoel of a field-collected EAB larva. (Photo credit: Deborah Miller); (d) P. sulcata cocoon in 

an EAB pupal chamber in the trunk of an ash tree. (Photo credit: Leah Bauer) 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Balcha indica (Eupelmidae) 

Balcha indica (Fig. 4a-c), native to Southeast Asia and 

naturalized in eastern United States, is occasionally 

found parasitizing EAB and other wood-boring 

beetles (Gibson, 2005). It is a solitary, ectoparasitic 

and parthenogenic idiobiont that parasitizes EAB 

larvae, prepupae, and pupae (Bauer et al., 2004; Duan 

et al., 2009). Adult females reared from woodborers 

in the United States vary in size from 3 to 8 mm long 

(Gibson, 2005). Duan et al. (2011a) studied its biology 

in the laboratory at 25 oC using adult females reared 

from parasitized EAB larvae collected in Pennsylvania 

(Duan et al., 2009). They found the generation time 

of B. indica averaged 83 days (range 47-129), which 

is slow compared to the development time of other 

EAB ectoparasitoids reared under similar conditions. 

Female fecundity averaged 36 eggs during an average 

59 day life span. These laboratory findings support 

field observations of one unsynchronized generation 

per year attacking immature EAB infested ash trees 

in Michigan, Pennsylvania, and Maryland (Duan 

et al., 2011a). As an established parasitoid of EAB 

and other woodborers in the United States, B. indica 

will continue playing a role in suppressing EAB 

population densities in North America (Duan et al., 

2014a). 

Biology oF parasitoids 

attaCKing eaB in eUrasia 

Several hymenopteran parasitoid species attack 

EAB larvae in Asia, as does one recently discovered 

attacking EAB in Europe (Table 1). In Asia, rates 

of EAB larval parasitism are consistently higher 

than those reported for EAB in North America. 

Tetrastichus planipennisi (Hymenop.: Eulophidae) is 

the dominant parasitoid of EAB larvae in northeast 

China (Liu, H-P. et al., 2003, 2007; Yang et al., 

2006). This parasitoid was also found attacking 

EAB in the Khabarovsk and Vladivostok regions of 

the Russian Far East (Duan et al. 2012b). In South 

Korea, an unidentified species of Tetrastichus was 

found parasitizing EAB larvae (Williams et al., 

2010). Other larval parasitoids of EAB in Asia are 

in the family Braconidae. Spathius agrili is the most 

a

b

c

Figure 4. Balcha indica life stages: (a) B. indica adult reared from 

an EAB prepupae in laboratory. (Photo credit: Houping Liu); 

(b) B. indica larva parasitizing an EAB larva in gallery. (Photo 

credit: Houping Liu); (c) B. indica cocoon with remnant of EAB 

host larva in gallery. (Photo credit: Houping Liu) 
CHAPTER 6: BIOLOGY OF EMERALD ASH BORER PARASITOIDS

103 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

prevalent parasitoid of EAB larvae in the vicinity of 

Tianjin, China, southeast of Beijing. It is also found 

sporadically in the northeastern provinces (Xu, 2003; 

Liu, H-P. et al., 2003; Yang et al., 2005; Wang et al., 

2010). In the vicinity of Vladivostok in the Russian 

Far East, both Spathius galinae Belokobylskij and 

Atanycolus nigriventris Vojnovskaja-Krieger parasitize 

EAB larvae (Williams et al., 2010; Belokobylskij 

et al., 2012; Duan et al., 2012b). Spathius galinae 

was also reported attacking EAB in South Korea. 

More recently, Spathius polonicus Niezabitowski, a 

braconid native to Europe, was discovered attacking 

EAB larvae in Moscow (Orlova-bienkowskaja 

and Belokobylskij, 2014). Another hymenopteran 

parasitoid, Sclerodermus pupariae Yang and Yao 

(Bethylidae) attacks EAB larvae and pupae in the 

region of Tianjin, China (Wu et al., 2008; Wang et al., 

2010; Tang et al., 2012; Yang et al., 2012). Due to a 

broad host range and tendency to sting humans, this 

species was not considered for EAB biological control 

in North America. 

Few egg parasitoids are known to attack EAB in 

Asia (Table 1). Oobius agrili (Hymenop.: Encyrtidae) is 

the most widespread parasitoid of EAB eggs and was 

first discovered in 2004 in Jilin province, China (Zhang 

et al., 2005). It is now known from other provinces 

in northeast China (LSB & JJD, unpublished data). 

More recently, a closely related species of Oobius was 

discovered in the Russian Far East (JJD, unpublished 

data) and an undescribed species of Oenycyrtus 

(Hymenop.: Encyrtidae) was reared from EAB eggs 

collected in Jilin province, China (LSB, unpublished 

data). 

Oobius agrili (Encyrtidae) 

Discovered in northeast China, O. agrili is a solitary 

parthenogenic parasitoid of EAB eggs. Due to its 

importance as a natural enemy of EAB in northeast 

China, where egg parasitism averaged 44% (Liu, H-P. et 

al., 2007), O. agrili was approved for use as a biological 

control agent of EAB in the United States in 2007 

(Federal Register, 2003). Establishment and spread is 

confirmed in Michigan and other states (Duan et al., 

2011b, 2012c; Bauer et al., 2013, 2014, in press). At six 

EAB biological control study sites in Michigan where 

researchers began monitoring EAB mortality following 

the first parasitoid releases in 2007, the level of egg 

parasitism by O. agrili increased from 0.7% to 22% 

from 2008 to 2012 (Abell et al., 2014). 

Oobius agrili (Fig. 5a-d) overwinter as diapausing 

prepupae inside EAB eggs, and adult eclosion is well 

synchronized with the oviposition period of EAB, 

starting in late June and continuing into September in 

China and Michigan (Liu, H-P. et al., 2007; Bauer and 

Liu, 2007; Abell et al., 2011). When O. agrili completes 

two generations per year, ~80% of the first generation 

progeny emerge and parasitize newly laid EAB eggs, 

whereas ~80% of the second generation enter obligate 

diapause for the winter. Moreover, the number of 

progeny entering diapause also increases as the female 

ages, and diapause may also be induced by exposure 

of adults to short day length (LSB, unpublished 

data). Consequently, O. agrili completes one or two 

generations per year (Liu, H-P. et al., 2007). Because 

this species is parthenogenic, only females are reared 

and released in the United States for EAB biological 

control. Males were recovered from parasitized EAB 

eggs collected in 2005 Jilin province, China; the sex 

ratio of adults reared from that sample was 15:1 

(female: male). In the laboratory when reared at 24oC, 

non-diapausing O. agrili complete one generation 

every 28 to 34 days, with an average fecundity of 80 

progeny per wasp. The average longevity of females 

exposed to eggs in the laboratory is 34 days (LSB, 

unpublished data). 

Tetrastichus planipennisi (Eulophidae) 

Native to regions of China and the Russian Far East, T. 

planipennisi is a gregarious endoparasitic koinobiont of 

EAB larvae. Due to its importance as a natural enemy 

of EAB in regions of Asia where larval parasitism 

averaged 22% (Liu, H-P. et al., 2007), T. planipennisi 

was approved for biological control of EAB in the 

United States in 2007 (Federal Register, 2007) and 

Canada in 2013 (CFIA, 2013). Its establishment and 

spread was confirmed in Michigan and other states 

(Bauer et al., 2014, in press; Gould et al. 2011a, 2013; 

Duan et al. 2013b, 2014a). At the six Michigan EABbiological control study sites where releases began in 

2007, researchers found EAB larval parasitism by T. 

planipennisi increased from 1.2% to 21% from 2008 to 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

a b

c d

Figure 5. Oobius agrili life stages. (a) O. agrili adult ovipositing in an EAB egg, as observed through a dissecting microscope. (Photo 

credit: Deborah Miller); (b) O. agrili-parasitized EAB egg (left) with early symptoms of O. agrili development, characterized by 

darkening coloration of egg, breathing tube and air bubble; a healthy, unparasitized EAB egg (right). (Photo credit: Deborah 

Miller); (c) O. agrili prepupa (left) and young, developing pupa (right) dissected from a field-collected parasitized EAB egg. (Photo 

credit: Houping Liu); (d) O. agrili-parasitized EAB eggs range in color from black (left) to tan (right, for comparison). Adult O. agrili 

chew a round exit hole on the dorsal surface of the egg to emerge. O. agrili meconium pellets are excreted prior to pupation and 

remain visible as dark beads inside a lighter colored parasitized egg (right). (Photo credit: Deborah Miller) 

Tetrastichus planipennisi (Fig. 6a-f) lacks obligate 

diapause and overwinters as prepupae inside host 

galleries or as young larvae inside host larvae. In 

northeast China and Michigan, adult emergence 

begins in April or May when females begin parasitizing 

overwintered EAB larvae ranging in age from second 

through fourth instar (Liu, H-P. et al., 2007; Duan et 

al., 2013a). After maturation, pupation, and eclosion, 

which all occur in the host gallery the following spring, 

adults chew small, round exit holes in the tree bark, 

emerge, and disperse. From field collections in Jilin 

province, China, T. planipennisi completed about four 

generations per year (Liu, H-P. et al., 2007). An average 

of 35 individual wasps (range 5 to 122) developed 

within a single host larva, with a sex ratio of 2.5:1 

(female: male) (Liu and Bauer, 2007; Liu, H-P. et al., 

2007). 

Tetrastichus planipennisi is a relatively small 

parasitoid (3 to 4 mm long) and may be more effective 

at parasitizing EAB larvae in small ash trees (<12 

cm DBH) with thin bark, due to its short ovipositor 

(2.0 to 2.5 mm long), than in large ash trees (Yang et 

al., 2006; Abell et al., 2012). The rate of spread of T. 

planipennisi in Michigan was estimated at >5 km per 

year between 2007 and 2010 (LB and JL, unpublished 

data). In the laboratory, T. planipennisi completes one 

generation every 27 days at 25 oC, has a sex ratio of 4:1 

(female: male), has an average realized fecundity of ~45 

female progeny per female; and has an average female 

longevity of 42 days (Ulyshen et al., 2010; Duan et al., 

2011b; Duan and Oppel, 2012). 

Spathius agrili (Braconidae) 

Known mainly from China southeast of Beijing, S. 

agrili is a gregarious ectoparasitic idiobiont of lateinstar EAB larvae (Xu, 2003; Liu, H-P. et al., 2003; 

Yang et al., 2005, 2010). Spathius agrili was approved 

for biological control of EAB in the United States 

in 2007 (Federal Register, 2007); however, in 2013 

APHIS restricted its release to regions below the 40th 

parallel because of a failure to establish further north 
CHAPTER 6: BIOLOGY OF EMERALD ASH BORER PARASITOIDS

105 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

a

b

c d

e f

Figure 6. Tetrastichus planipennisi life stages (a) adult female (Photo credit: David Cappaert; (b) Young T. planipennisi larvae 

are visible inside an emerald ash borer larva. (Photo credit: Deborah Miller); (c) Mature T. planipennisi larvae completing 

development inside an emerald ash borer larva. (Photo credit: Houping Liu); (d) Fully mature T. planipennisi larvae break free of 

emerald ash borer larval skin and pupate in the larval gallery under the tree bark. (Photo credit: Clifford Sadof ). (e) T. planipennisi 

pupae in emerald ash borer larval gallery. (Photo credit: Houping Liu). (f ) After eclosion to the adult stage in emerald ash borer 

galleries, adult T. planipennisi chew an exit hole to emerge from the ash trees (with tip of pen for scale). (Photo credit: Leah Bauer) 
CHAPTER 6: BIOLOGY OF EMERALD ASH BORER PARASITOIDS

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

(Bauer et al., 2014, in press; Gould et al., 2011a,b; 

2013;USDA APHIS/FS/ARS, 2013). 

Spathius agrili (Fig. 7a-d) overwinter as mature 

larvae or prepupae in silken cocoons, emerge as 

adults in July and August and complete one or two 

generations per year, with a clutch size of 5 to 6 

individuals per EAB larva (Wang et al., 2006, 2008; 

Gould et al., 2011a). In the laboratory when reared 

at 25:20 oC (day:night temperature cycles) and 16:8 

(light:dark photoperiod), the sex ratio of S. agrili 

averaged 4:1 (female: male), and an average fecundity 

of ~40 female progeny per female. The average 

longevity of females is 61 days (Gould et al., 2011a). 

Spathius galinae (Braconidae) 

Spathius galinae (Fig. 8), recently discovered in the 

Russian Far East and reported in South Korea, is a 

gregarious, ectoparasitic idiobiont of EAB larvae 

(Williams et al., 2010; Belokobylskij et al., 2012; Duan 

et al., 2012b). When reared in the laboratory at 25 °C 

and 16:8 (light:dark photoperiod), S. galinae develops 

from egg to adult in about a month and completes with 

one generation per year; female longevity averages 49 

days and produce an average of 31 progeny in clutches 

ranges in size from 5 to 12 individuals per EAB larva 

(Duan et al. 2014b). Due to better climate matching 

of the Russian Far East with northern regions of the 

a b

c d

Figure 7. Spathius agrili life stages: (a) S. agrili adult female. (Photo credit: Tracy Ayers); (b) S. agrili eggs on an emerald ash borer 

larva. (Photo credit: Zhong-qi Yang); (c) S. agrili larvae feeding externally on an emerald ash borer larva. (Photo credit: Houping 

Liu); (d) S. agrili cocoons in emerald ash borer larval gallery. (Photo credit: Houping Liu) 
CHAPTER 6: BIOLOGY OF EMERALD ASH BORER PARASITOIDS

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Figure 8. Spathius galinae adult female ovipositing in an ash 

log. (Photo credit: Jian Duan) 

United States and narrow host specificity, researchers 

requested permission to release S. galinae as an EAB 

biological control agent in the United States in 2014. 

ConClUsions 

Although EAB is attacked by a diversity of native 

parasitoids of wood-boring beetles in North America, 

their prevalence is relatively low compared to that 

of the EAB-parasitoid complex in northeast Asia, 

where this buprestid originated. Consequently, classical 

biological control of EAB, with the introduction of 

three parasitoid species from China, was initiated in 

Michigan in 2007. By 2012, the establishment and 

increasing prevalence of two introduced parasitoids, T. 

planipennisi and O. agrili, was confirmed in Michigan 

and several other states. Besides increasing parasitism 

by the introduced and native parasitoid species, other 

important mortality factors are now known to suppress 

EAB population densities including host resistance 

in healthy ash trees, woodpecker predation, and 

entomopathogens. With the continued persistence 

of EAB and ash in the environment, we expect a 

cumulative effect of biotic and abiotic mortality factors 

to suppress EAB population densities below a tolerance 

threshold, ensuring the survival and reproduction 

of some native ash. The continuation and expansion 

of long-term field studies in EAB-infested forest 

ecosystems, where EAB biological control agents are 

released, is essential for further development of an 

integrated pest management approach to EAB in North 

America. 

reFerenCes 

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R. G. Van Driesche. 2011. Assessment of Oobius 

agrili phenology using egg sentinel logs, pp. 

99–100. In: Mastro, V., D. Lance, R. Reardon, 

and G. Parra (compilers). Proceedings of the 2011 

Emerald Ash Borer Research and Development 

Review Meeting, Wooster, Ohio. USDA Forest 

Service FHTET-2011-06, Morgantown, West 

Virginia, USA. http://www.fs.fed.us/foresthealth/ 

technology/pdfs/EAB_FHTET-2011-06.pdf 

Abell, K. J., L. S. Bauer, J. J. Duan, and R. G. Van 

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FHTET-2007-04, Morgantown, West Virginia, 

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Chapter 7: trapping teChniqUes For emerald ash Borer and its introdUCed parasitoids 

Kristopher Abell1,3, Therese Poland2,3, Allard Cossé4 and Leah Bauer2,3 

1

Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts 01003
 

2

USDA Forest Service, Northern Research Station, East Lansing, Michigan 48823
 

3

Department of Entomology, Michigan State University, East Lansing, Michigan 48824
 

4

USDA ARS, National Center for Agricultural Utilization Research, Peoria, Illinois 61064
 

sUrvey and deteCtion 

oF emerald ash Borer 

As soon as emerald ash borer (Agrilus planipennis 

Fairmaire) (EAB) was discovered near Detroit, 

Michigan, USA, in 2002, surveys were initiated to 

delimit the extent of the infested area. These initial 

delimitation surveys were based on visual assessments 

using external symptoms because at the time no other 

detection tools were available and nothing was known 

about EAB responses to chemical or visual stimuli. 

Surveys were supplemented by tracing movement of 

nursery stock shipped from Detroit to other locations 

to detect new infestations of EAB. External symptoms 

of EAB infestation, which include D-shaped exit holes, 

dieback and crown thinning, epicormic shoots, and 

bark splits over galleries, are not apparent until one or 

more years after trees are infested by which time some 

adult beetle emergence may have occurred, allowing 

dispersal to other locations (Poland and McCullough, 

2006). Therefore, visual surveys that rely on detecting 

infested trees are not effective for discovery of lowdensity infestations. 

As of 2014, development of better detection 

tools for EAB remained an important need for the 

regulatory program. Research on EAB behavior 

demonstrated that adult beetles respond to volatiles 

emitted by stressed ash (Rodriguez-Saona et al., 

2006) and preferentially oviposit on girdled trees 

(McCullough et al., 2009a,b). Based on this finding, 

in 2004 the Michigan Department of Agriculture 

implemented a statewide survey employing grids of 

girdled trap trees (Rauscher, 2006; Hunt, 2007). Large, 

open-grown ash trees were girdled in spring before 

EAB emergence by removing a band of bark and 

phloem, approximately 16 cm wide, around the whole 

circumference of the tree. A band of plastic 

wrap, approximately 30 cm wide, was placed on the 

trunk above the girdle and coated with Tanglefoot 

insect trapping glue. Girdled trap trees were visually 

inspected during the summer to detect EAB adults 

on sticky bands; in fall or winter, girdled trees were 

felled and sections of the log were peeled to locate 

EAB larvae or galleries. Grids of over 10,000 trap 

trees were used for detection surveys in Michigan 

and several surrounding states up through 2008. 

While girdled trees are the most effective tool for 

detecting EAB (McCullough et al., 2011; Mercader et 

al., 2013), debarking trees to locate larval galleries is 

costly and labor-intensive, and suitable trees are not 

always available. Consequently, emphasis was placed 

on development of traps and lures that incorporated 

visual or olfactory cues to attract and capture EAB 

adults. 

Odors from the leaves of stressed ash trees 

(Rodriguez-Saona et al., 2006), green leaf volatiles, 

especially cis-3-hexenol (de Groot et al., 2008; Grant et 

al., 2010, 2011; Poland et al., 2011), and sesquiterpene 

volatiles from ash bark elicit antennal responses 

and are attractive to EAB. Many of these attractive 

compounds are present in a natural tree oil called 

Manuka oil (Crook et al., 2008), and for this reason 

this oil was often incorporated into EAB traps. 

Male and female EAB are sensitive to light in 

the ultraviolet (UV), violet, and green (420-430, 

460, and 530-560 nm, respectively) ranges of the 

electromagnetic spectrum, while mated females are 

also sensitive to light in the red (640-670 nm) range 

(Crook et al., 2009, 2012). The beetles are attracted to 

green or purple traps hung in both the open and the 

ash canopy (Crook et al., 2009; Francese et al., 2010). 
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a b c

d e

Figures 1 a-d. Various trap designs, colors and lure combinations suspended in the canopy of an ash tree: .(a) Dark purple sticky 

prism trap. (Photo credit: Therese Poland); (b) Light sabic purple sticky prism trap. Photo credit: Therese Poland); (c) Green 

multiple funnel trap coated with Fluon. (Photo credit: Toby Petrice); (d) Green sticky prism trap. (Photo credit: Therese Poland); 

(e) Green and purple double decker trap. (Photo credit: Therese Poland) 

Males, which tend to hover near the canopy of ash 

trees (Rodriguez-Saona et al., 2007), are captured in 

higher proportions in green traps hung in the canopy 

of ash trees and baited with green leaf volatiles; in 

contrast, females, that oviposit on the trunks of ash 

trees are captured in higher proportions in purple 

traps hung below the canopy and baited with bark 

sesquiterpenes (Crook and Mastro, 2010; Grant et 

al., 2011). There is also evidence that close range or 

contact pheromones are involved in mate recognition 

and mating behavior (Lelito et al., 2009; Pureswaran 

and Poland, 2009) and that a female-produced volatile 

pheromone, cis-lactone, increases attraction of males 

to green canopy traps baited with green leaf volatiles 

(Silk et al., 2009, 2011; Ryall et al., 2012). 

Artificial traps were first used by USDA Animal 

Plant Health Inspection Service (APHIS) in a national 

EAB detection survey in 2008 (Crook and Mastro, 

2010). Traps consisted of 3-sided prisms made of 

standard dark purple corrugated plastic (Coroplast 

Inc., Dallas, TX; 421 nm, 16.3% reflectance; 605 nm, 

9.5%; 650 nm, 14.2%). Traps were coated with clear 

insect trapping glue, hung in the canopy of ash trees, 

and baited with Manuka oil lures with release rates 

of 50 mg/day (Synergy Semiochemicals, Burnaby, 

B.C.) (Fig. 1a). Various trap designs, colors, and lure 
CHAPTER 7: TRAPPING TECHNIQUES FOR EAB AND ITS PARASITOIDS

115 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

 

 

 

combinations were tested and detection surveys 

modified to incorporate the latest research findings. 

Starting in 2014, a new lighter shade of purple (Great 

Lakes IPM, Vestaburg, MI; Sabic purple, 413 nm, 

32.8%; 613 nm, 18.8%; 650 nm, 28.5%) was employed 

for the sticky prism traps hung in the canopy of ash 

trees. Also, cis-3-hexenol lures releasing 50 mg/day 

(Scentry Biologicals, Inc., Billings, MT) have been 

added to the Manuka oil lures (USDA APHIS, 2014) 

(Fig. 1b). 

Other promising traps under evaluation as of 2014 

included (1) green (530 nm, 57% reflectance) multiple 

funnel traps (Chemtica Internacional, San Jose, Costa 

Rica) coated with Fluon, a slippery polymer (Northern 

Specialty Chemicals, Dudley, MA), and baited 

with cis-3-hexenol released at 50 mg/day (Scentry 

Biologicals, Inc., Billings, MT) (Francese et al., 2011) 

(Fig. 1c), (2) green (540 nm, 49% reflectance) sticky 

prism traps hung in the canopy of ash trees baited 

with cis-3-hexenol and the EAB pheromone cislactone (Sylvar Technologies, Inc., Fredericton, NB) 

(Ryall et al., 2012) (Fig. 1d), and (3) double decker 

traps made of a 10 foot PVC pole to which a green 

sticky prism (540 nm, 49% reflectance) is attached 

at the top and a light purple sticky prism (413 nm, 

32.8%; 613 nm, 18.8%; 650 nm, 28.5%) is attached 60 

cm below (Great Lakes IPM, Vestaburg, Michigan); 

both prisms are baited with two cis-3-hexenol bubble 

caps releasing 3.7 mg/day per bubble cap (ConTech 

Enterprises, Inc., Delta, B.C) (Poland et al., 2011, 

Poland and McCullough, 2014) (Fig. 1e). 

The 2014 national emerald ash borer survey 

included (1) a nationwide survey of 8800 traps, set 

outside the 100 mile wide buffer zone surrounding 

the known infested area in locations at risk for 

introduction and establishment of EAB and (2) a 

leading edge survey employing 13,200 traps set within 

the 100 mile wide buffer zone. Traps were set within 

1 km2

 cells that were selected using a risk-based 

model that incorporated risk factors that included 

proximity to campgrounds, major transportation 

arteries, truck stops, sawmills, firewood vendors, tree 

nurseries, recently landscaped properties, and high 

attendance cultural event sites. A trap was placed 

within each 1 km2

 cell, avoiding habitats of threatened 

or endangered species. Traps were placed in the 

lower to mid-canopy of ash trees, preferably 20 cm 

or more in diameter, along edges or open areas on 

the sunny side of trees. The bottom edge of the trap 

was 150 cm or more above ground (USDA APHIS, 

2014). In addition, any ash trees within each 1 km2 

cell exhibiting two or more symptoms of emerald ash 

borer infestation (dieback, epicormic shoots, bark 

splits, woodpecker damage, D-shaped exit holes, 

or visible serpentine galleries) were destructively 

sampled by removing bark to reveal emerald ash borer 

galleries and larvae. 

Traps were placed in the field just before 250 

growing degree days (base 10 °C) were accumulated, 

which corresponds approximately to the time when 

emerald ash borer emergence begins. Lures were 

replaced within 60 days. Traps were checked at a 

minimum when lures were replaced and when traps 

were taken down. All captured EAB and suspect 

beetles were collected and submitted to the State Plant 

Health Director or APHIS representative for species 

determination. Traps remained in place until after 

August 1 and 833 growing degree days (base 10 °C) 

had accumulated (USDA APHIS, 2014). 

sUrvey and deteCtion oF 

introdUCed eaB parasitioids 

For parasitoids introduced for biological control, 

both their establishment and impact on the target 

pest must be measured. Establishment means the 

development of a successfully reproducing, selfsustaining population of the natural enemy, complete 

with overwintering survival for one or more years. 

Parasitoid establishment cannot be determined until 

at least one year after parasitoid release. Evaluating 

the impact of a natural enemy on the population of 

the target pest requires an estimate of the mortality 

caused by the natural enemy to the host; often this 

is equivalent to the generational rate of percentage 

parasitism in the naturally occurring host population 

in the field. Some parasitoids can kill hosts by means 

other than parasitoid reproduction, such as host 

feeding or stinging hosts without laying any eggs 

(DeBach, 1943; Van Driesche and Taub, 1983; Jervis 

and Kidd, 1986; Kidd and Jervis, 1989; Heimpel 

and Collier, 1996; Jervis et al., 1996); however, the 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

a b

Figure 2 a,b. Laboratory produced emerald ash borer eggs on bark flakes placed under bark flaps cut into ash trees in the field. 

(Photo credit: Jian Duan) 

parasitoids currently being released against emerald 

ash borer do not have these behaviors. 

In the case of the emerald ash borer, there are 

two beetle life stages targeted by parasitoids: the 

egg and larva. The egg parasitoid, Oobius agrili 

Zhang and Huang (Hymenoptera: Encyrtidae) 

(Zhang et al., 2005) and two larval parasitoids, 

Tetrastichus planipennis Yang (Eulophidae) (Yang et 

al., 2006) and Spathius agrili Yang (Hymenoptera: 

Braconidae) (Yang et al., 2005), have been imported 

and released in North America (Bauer et al., 2008). 

Various methods have been developed to assess the 

establishment and impact of these parasitoids and 

they are reviewed in this chapter. 

egg parasitoids 

Three approaches have been used to detect 

establishment or measure the impact of the egg 

parasitoid O. agrili: (1) deploying laboratoryproduced host eggs in the field as sentinel eggs, (2) 

using yellow pan traps to passively collect O. agrili 

adults, and (3) collecting wild (naturally occurring) 

emerald ash borer eggs in the field. 

Sentinel Eggs 

Deployment of sentinel eggs can detect the presence 

of O. agrili at particular sites, which, if appropriately 

timed, can indicate establishment. Several methods 

have been developed for field-deployment of emerald 

ash borer eggs produced in the laboratory. The first 

of these involves cutting a small flap of bark on an 

ash tree and placing EAB eggs under this flap (Fig. 

2). Eggs can be collected later and examined for 

parasitism. This method, however, suffers from a 

high degree of egg predation (Duan et al., 2011). The 

second method is based on the field-deployment of 

ash logs bearing laboratory-laid EAB eggs. These egg 

sentinel logs (ESL) are made by wrapping curling 

ribbon around a bolt of ash (ca 5 cm in dia by 25 cm 

long) and placing them in a container with gravid 

EAB for several days (Fig. 3). The tight space between 

the curling ribbon and the ash bolt stimulates 

EAB oviposition (Fig. 4) and partially conceals the 

egg from predators in the field. A more detailed 

description of ESL production can be found in Duan 

et al. (2012a) and USDA APHIS/ARS/FS (2013). 

Once produced, ESL units can be hung on or near ash 

trees and left for several weeks. It should be noted, 

however, that depending on temperature EAB eggs 

are only suitable for parasitism up to the development 

of the neonate host larva (approximately 8-10 days 

after oviposition). Once collected from the field, eggs 

on ESL units can be held in the laboratory to rear O. 

agrili adults. Alternatively, each egg can be inspected 

under a microscope for visual signs of parasitism (Fig. 

5). A third method of deploying sentinel eggs is to 

place host eggs inside various protective enclosures, 

such as plastic cups (with or without a screened 

opening) or pouches made entirely of screening. 

Screening is used to exclude predators while allowing 

access to eggs by O. agrili. While field recoveries 

of O. agrili have been made using this method, it 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

Figure 3. Egg sentinel log with curling ribbon in container with Figure 4. Egg sentinel log with curling ribbon removed 

emerald ash borer. (Photo credit: Deborah Miller) showing EAB eggs. Black eggs are parasitized and brown eggs 

are unparasitized. (Photo credt: Kristopher Abell) 

a b

Figure 5. (a) Parasitized EAB egg with parasitoid emergence hole and typical black coloration. (b) Parasitized EAB egg with 

meconium inside visible due to atypical brown coloration. (Photo credit: Deborah Miller) 

generally seems less effective compared to use of 

ESL units. Currently, therefore, of the three methods 

used to deploy emerald ash borer eggs in the field to 

detect egg parasitism, use of sentinel egg logs is the 

preferred method (Fig. 6). 

Yellow Pan Traps 

Yellow pan traps are yellow plastic bowls (Fig. 7) 

mounted to ash trees with a shelf bracket nailed to the 

tree. A second bowl can be placed inside the mounted 

bowl to allow for easy removal and processing of the 

sample. This second bowl is filled with a 20% clear 

propylene glycol solution and a drop of unscented 

detergent. Yellow bowls are used because this color is 

generally attractive to many parasitoids, and detergent 

decreases the surface tension of the water, causing 

most insects to sink and drown. Trap contents 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

Figure 6. Egg sentinel log suspended from an ash tree in the Figure 7. Yellow pan trap. (Photo credit: Leah Bauer) 

field. (Photo credit: Kristopher Abell) 

a b

Figure 8 a,b. Emerald ash borer eggs on ash bark in the field. (Photo credit: Jian Duan) 

Figure 9. Removal and collection of outer ash bark with a Figure 10. Emergence tubes used to collect emerging Oobius 

drawknife for assessment of Oobius agrili using emergence agrili from bark samples. (Photo credit: Deborah Miller) 

tubes and bark sifting. (Photo credit: Kristopher Abell) 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

should be collected after several days depending on 

temperature to avoid rotting. Once collected, the 

contents of the pan trap can be examined for the 

presence of O. agrili adults (JG, unpublished data). A 

detailed step-by-step guide to the construction and 

setup of yellow pan traps can be found in “Emerald 

Ash Borer Biological Control Release and Recovery 

Guidelines” (USDA APHIS/ARS/FS, 2013). Yellow 

pan traps are non-selective and may not detect low 

density populations of O. agrili. 

Naturally Occurring EAB Eggs 

Assessing the impact of O. agrili (i.e., percent 

parasitism for EAB populations) is a more difficult 

task than determining if O. agrili is established at 

a site. To assess the impact of O. agrili on naturally 

occurring EAB egg populations, EAB eggs must be 

collected in the field. Finding EAB eggs in the field is 

difficult because adults lay their eggs between layers 

of bark or in bark fissures on ash trees (Fig. 8). Two 

methods have been developed to collect wild EAB 

eggs. The first collection process is a timed visual 

inspection of ash bark, using a utility knife to parse 

away bark layers. An arbitrary but fixed amount of 

time (generally 30 minutes) is spent searching each 

tree to maintain consistent sampling effort. Eggs found 

are returned to the laboratory to be inspected with a 

dissecting microscope for signs of parasitism (Fig. 5) 

(Duan et al., 2011, 2012a). 

A second method to measure rates of parasitism 

in wild EAB eggs is based on the physical removal of 

the outer bark of ash trees over a fixed area, inside of 

which layers of bark are scraped off using a drawknife 

(Fig. 9). If assessing establishment is the only goal, 

then sampled bark can be placed in emergence tubes 

(Fig. 10) and monitored for O. agrili emergence. 

Emergence tubes are typically made from cardboard 

mailing tubes, but other light-excluding containers 

can be used. One end of the tube is sealed against light 

while an inverted funnel and translucent collection 

cup (Fig. 11) is mounted on the other end. Tubes 

should be held in a well lit environment at 18-32 °C. 

At low densities, O. agrili may be difficult to detect 

because the parasitoids do not always find their way 

out of the emergence tube and into the collection 

cup. A more reliable way to detect O. agrili in bark 

Figure 11. Close-up view of Oobius agrili emergence tube, cup 

and funnel. (Photo credit: Deborah Miller) 

Figure 12. Sifting bark samples using standard nylon window 

screening. (Photo credit: Deborah Miller) 

samples, which also allows for assessment of impact, 

is to examine the collected bark. While a complete 

search of the entire bark sample would be the most 

effective, it takes too long. Therefore, a subsampling 

approach was developed that involves sifting the 

bark sample with standard nylon window screening 

and determining rates of parasitism in eggs that pass 

through the screen. The bark sample is placed on 

window screening and shaken for three minutes (Fig. 

12). Many eggs are dislodged while shaking and fall 

through the openings in the screening along with 

small bits of bark debris. The material that passes 

through the sieve is then examined for EAB eggs 

using a microscope, and each egg is evaluated for 

parasitism. An estimate of percent parasitism can be 

obtained from each of these methods (timed visual 

search and bark sifting) by dividing the number 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

of parasitized eggs by the total number of eggs 

(parasitized and not, both emerged and not emerged, 

live and dead). 

Advantages and Disadvantages of Methods 

for Detection of Egg Parasitoids 

The use of sentinel eggs, whether under bark flaps, 

on ESL units, or in protective enclosures, is subject 

to predation. Very often predators may remove most, 

or even all, sentinel eggs. The presence of curling 

ribbon on the logs used in the ESL units and screening 

over protective enclosures around the ESL unit both 

reduce but do not eliminate predation. Additionally, a 

substantial amount of infrastructure and manpower is 

needed to maintain an EAB colony, which is required 

to produce eggs for field deployment. When creating 

ESL units, a sufficient number of eggs (~50-100) must 

be produced per log and deployed in the field within 

2-3 days. Older eggs are not preferred for parasitoid 

oviposition and their deployment produces little 

useful data. Time of deployment of sentinel eggs 

must also be carefully considered to coincide with 

seasonal occurrence of O. agrili adults. Deployment 

of sentinel eggs too early or too late in the year would 

result in false negatives when assessing establishment. 

In Michigan, O. agrili adult females first appear after 

approximately 445-556 degree days (base 10 °C) (Abell, 

unpublished data). 

Yellow pan traps may be a relatively easy method 

to assess establishment of O. agrili. Unlike methods 

using sentinel eggs, pan traps do not require the 

maintenance of an EAB colony to produce eggs and 

the time constraints associated with egg viability 

are not an issue. Furthermore, since pan traps have 

the potential to also catch larval parasitoids of EAB 

this may increase their utility. However, there are 

several important disadvantages to consider. First, 

the incidental trap-catch of other similar-looking 

hymenoptera or other insects can be substantial. When 

such incidental catch is high, more time is required 

to examine and sort through the sample, which is 

particularly difficult considering the small size of O. 

agrili. Because of its small size, O. agrili can often 

become entangled in the setae of other insects making 

them easy to miss. Second, the effectiveness of yellow 

pan traps is largely unknown. Some work has shown 

pan traps to be more effective than ESL units and other 

sentinel egg methods, while other work has shown 

the opposite (Parisio, unpublished data; Bauer et al., 

2011a). 

Timed visual egg surveys and bark sifting allow for 

assessment of establishment and estimation of percent 

parasitism of naturally occurring field populations, 

but each has disadvantages to consider. Both methods 

collect EAB eggs from several generations and there 

is no way to differentiate old eggs from new ones. 

Because of this it can be difficult to assess yearto-year fluctuations in rates of parasitism at a site. 

Consideration of aspect (cardinal direction) of the 

sampling point on the tree is also important for each 

method. Sampling from only one side of a tree may 

introduce a bias. In general, sampling around the 

full circumference of the tree is recommended for 

estimating field rates of parasitism. However to only 

estimate establishment, egg density and parasitism 

rates are greatest on the south and west sides of tree 

(Abell et al., 2014). Visual egg surveys have several 

special disadvantages: finding eggs on standing ash 

trees in the field is difficult even with the aid of a 

magnifying lens, searching is affected by light and 

weather conditions in the field, and the process of 

removing small bits of bark while searching likely 

results in the loss of some eggs along with the removed 

bark. The bark sifting method does not have these 

disadvantages, but is more time consuming. 

Regardless of the method used, O. agrili is 

particularly challenging to sample. Work done using all 

the above methods has shown that, at least during the 

first several years following the species release at a site, 

O. agrili has a very patchy distribution. Often, only 10­

20% of trees sampled within several hundred meters of 

each other will result in recovery of O. agrili (Abell et 

al., 2011). Therefore a large number of trees (>10) need 

to be sampled to adequately assess O. agrili levels. 

larval parasitoids 

Several methods have been used to detect 

establishment and assess impact of larval parasitoids 

of emerald ash borer: (1) deployment of laboratoryreared EAB larvae in the field as sentinels, (2) using 

yellow pan traps to passively collect adult parasitoids, 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

and (3) collecting naturally occurring EAB larvae in 

the field for dissection or rearing. 

Sentinel Larvae 

There are several methods that employ sentinel larvae 

to assess establishment of parasitoids of emerald ash 

borer larvae. Larval sentinel logs (LSL) are similar 

in concept to the ESL units described previously for 

detection of the egg parasitoid. To construct LSL 

units, third to fourth instar EAB larvae are inserted 

into ash bolts approximately 5 cm in diameter and 

25 cm long. Bolts are sealed on both ends with 

paraffin wax to prevent desiccation. To insert larvae, 

a portion of inner bark and wood approximately 

the same size as an EAB larva is excavated from the 

log, and an EAB larva is placed in the grove and 

covered by the remaining flap of outer bark (Fig. 13). 

Several EAB larvae can be inserted into a bolt in this 

manner. Then, after the outer bark flaps are secured, 

the area of the log where a larva has been inserted is 

further protected by wrapping it with parafilm. Care 

should be taken to sterilize the tools used to create 

excavations and handle larvae to avoid introducing 

pathogens. LSL units are then placed on ash trees 

in the field (Fig. 14) and left in place for 1-2 weeks. 

How long LSL units last in the field depends upon the 

age of EAB larvae and the temperature. Since EAB 

larvae tunnel into the heartwood of ash to pupate, 

they become inaccessible to parasitoids at that point. 

Temperature affects the rate of development of EAB 

larvae; also higher temperature increases desiccation 

of LSL units. LSL units can also be produced by 

placing emerald ash borer eggs on ash bolts and 

allowing newly hatched larvae to bore into bolts; bolts 

are then held at a constant temperature until larvae 

reach the appropriate instar. This second method, 

however, is less desirable because the number of EAB 

larvae in each bolt will be unknown since some eggs 

won’t hatch and some larvae will die. In addition, 

LSL units produced in this manner seem to be less 

effective at detecting parasitism, possibly because cuts 

made when inserting larvae emit volatiles that attract 

parasitoids (Abell, unpub.). These two methods – 

inserting larvae or affixing eggs to bark – can also be 

applied to live ash trees in the field (Ulyshen et al., 

2010; Abell et al., 2012). Additionally, adult EAB can 

Figure 13. EAB larvae placed in excavated area of an ash bolt 

to create a larval sentinel log. (Photo credit: Kristopher Abell) 

Figure 14. Larval sentinel log hung on an ash tree in the field. 

(Photo credit: Kristopher Abell) 

be caged directly onto the trunk of live ash trees and 

allowed to oviposit eggs (Duan et al., 2014). 

Yellow Pan Traps 

The setup, advantages, and disadvantages of pan traps 

to capture EAB larval parasitoids are much the same 

as when they are used to detect egg parasitoids, as 

described above. As stated above, yellow pan traps 

are non-selective and may not detect low-density 
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populations of released EAB larval parasitoids. 

Recently the pheromones of Spathius agrili, Spathius 

floridanus Ashmead, and T. planipennisi have been 

identified (Bauer, et al., 2011b, Cossé et al., 2012), 

and these materials can be used as attractants in 

combination with yellow pan traps to increase 

trapping efficiency. 

The pheromones for the two Spathius species are 

male-produced aggregation pheromones attracting 

both male and female insects. The pheromone for 

T. planipennisi is a female-produced sex pheromone 

attracting males. 

The attractiveness of synthetic S. agrili pheromone 

was tested in a large (3.7 x 6.1 x 3.7 m) outdoor field 

cage using eight (1.8 m high) evenly spaced potted 

evergreen ash (Fraxinus uhdei [Wenz.] Lingelsh.) 

plants. Yellow sticky board strips (Fig. 15) were 

placed in each plant halfway up. The pheromone was 

impregnated into rubber septa, affixed to the sticky 

boards. Approximately 45% of the released males 

and 50% of the released females were recaptured on 

the pheromone-baited traps during the 24 h trapping 

periods (Fig. 16) (Cossé et al., 2012), compared to 

10% of released males and 5% of released females for 

yellow traps without pheromones. Field trapping of 

S. agrili using yellow pan traps and pheromone has 

not yet been demonstrated due to a lack of established 

populations of S. agrili. 

For T. planipennisi, wind tunnel behavioral studies 

have demonstrated that male T. planipennis are highly 

sensitive to a female-produced pheromone with 

optimal responses to pheromone at 20 pg/μl. Under 

summer conditions, this dosage of pheromone is likely 

to be attractive for T. planipennisi males for at least two 

weeks. A field test was run in August-September, 2013 

in East Lansing, Michigan where T. planipennisi has an 

established population. Twenty yellow pan traps were 

deployed following the method described, ten with 

and ten without pheromone lures. Septa were replaced 

by fresh ones after two weeks. Of 40 males trapped, 

39 were captured by pheromone-supplemented traps, 

while control traps (yellow only) caught one parasitoid 

(Fig. 17). 

The above results demonstrate that EAB parasitoid 

pheromones can increase efficiency of yellow pan 

traps. Pheromones of Spathius sp. and T. planipennisi 

Figure 15. Field cage setup for release and recapture of male 

and female Spathius agrili with yellow sticky traps baited with 

parasitoid pheromone. (Photo credit: Allard Cossé) 

are stable under field conditions and only small 

amounts of the pheromones are needed to attract 

the target parasitoids. A disadvantage of using 

pheromones is that they will have to be synthesized, 

since the compounds are not commercially available. 

Naturally Occurring EAB Larvae 

Sampling naturally occurring EAB larvae is the 

only way to estimate percent parasitism by larval 

parasitoids. To collect EAB larvae, the bark of living 

EAB infested ash trees is peeled off, usually with a 

drawknife (Fig. 18). Larvae can then be examined 

in the field or taken back to the laboratory to be 

dissected or reared to detect parasitoids (see Chapter 6 

for pictures and descriptions of parasitoid life stages). 

Several studies have demonstrated the effectiveness of 

this method (Duan et al., 2012b, 2013a,b, 2014). 

Advantages and Disadvantages of Methods 


for Detection of Larval Parasitoids
 

Similar to the use of sentinel eggs, deployment of 

sentinel larvae requires substantial infrastructure 

and manpower. EAB must be reared from the egg 

to 3rd or early 4th instar larval stage to be suitable for 

use. Predation of sentinel larvae is not a problem, but 

bacterial or fungal contamination can be, and once 

introduced into colonies, pathogens can become 

pervasive and difficult to eliminate. Additionally, 

un-infested ash is needed both for rearing EAB larvae 

and creating LSL units. Finding un-infested ash of the 
CHAPTER 7: TRAPPING TECHNIQUES FOR EAB AND ITS PARASITOIDS

123 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Figure 16. Percentage (± SE) of captured virgin male and female Spathius agrili 

on yellow sticky traps baited with pheromone. 

Figure 17. Total number of trapped male and female Tetrastichus planipennisi 

on yellow pan traps baited with pheromone. 
CHAPTER 7: TRAPPING TECHNIQUES FOR EAB AND ITS PARASITOIDS

124 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Figure 18. Peeling bark from ash trees to search for naturally 

occurring emerald ash borer larvae. (Photo credit: Leah Bauer) 

appropriate size can be difficult, especially in regions 

where EAB is abundant. Also, native parasitoids that 

attack EAB, such as Atanycolus spp. (Hymenoptera: 

Braconidae), sometimes attack many of the sentinel 

larvae, thus preventing assessment of introduced 

parasitoids. Despite these disadvantages, sentinel 

larvae allow for standardized, nondestructive detection 

of larval parasitoids. In addition, sentinel larvae can 

be deployed at any time during the field season. It 

is important, however, to deploy them when larval 

parasitoids are likely to be present (May-September). 

Sampling naturally occurring EAB larvae by 

peeling the bark of infested trees eliminates the need 

to rear and maintain EAB larvae, which must be done 

for sentinel larval methods. It also allows for the direct 

assessment of what is currently occurring in the field 

and estimation of attack rates by larval parasitoids. 

Bark peeling is destructive, however, so unlike the use 

of sentinel larval methods, in plots where there is a 

need for repeated sampling, collection of wild larvae 

must be limited to preserve trees for future work. 

Peeling bark is laborious and requires careful technique 

to avoid damaging larvae, since damaged larvae are 

often difficult to diagnose for parasitism, particularly 

for ectoparasites like Spathius spp. and Atanycolus spp., 

which can easily be dislodged and lost. In addition, 

cases in which larval parasitoids have already emerged 

are often difficult to diagnose. Finally, woodpecker 

predation can be high (Lindell et al., 2008; Duan et al., 

2012b, 2013a, 2014; Jennings et al., 2013), and it is not 

possible to determine if larvae taken by woodpeckers 

were also parasitized or not. 

reFerenCes 

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Chapter 8: mass-rearing oF emerald ash Borer and its parasitoids 

Jonathan P. Lelito1, Timothy J. Watt2, and Jian J. Duan2 

1

USDA APHIS PPQ, Brighton, Michigan 48116 


2

USDA ARS Beneficial Insects Introduction Research Unit, Newark, Delaware 19713
 

introdUCtion 

Mass rearing of emerald ash borer (EAB) (Agrilus 

planipennis Fairmaire) (Coleoptera: Buprestidae) poses 

significant challenges both in terms of understanding 

its biology and phenology in the field and maintaining 

sources of insect material in the laboratory. 

Fortunately, in the past few years, significant progress 

has been made by several USDA facilities on 

optimizing laboratory rearing of emerald ash borer for 

a variety of purposes (Duan et al., 2013ab). 

Rearing the natural enemies of wood boring 

insects is difficult because of the need for effective 

means to mass rear the host, which has a long (one 

or two year) life cycle and cryptic life history. At the 

initiation of any biological control program for a newly 

detected invasive wood boring pest such as EAB, 

information on the target pest as well as its natural 

enemies may be very limited. Using the emerald ash 

borer/parasitoid system as an example, the three 

primary natural enemies, now being produced and 

released across the United States, were newly described 

in the first several years following an intensive foreign 

exploration program (USDA APHIS, 2007) in response 

to the detection of the borer by federal agencies. 

At their simplest, the critical resources required 

for mass production of natural enemies of emerald ash 

borer are growth chambers with good temperature, 

humidity, and photoperiod control, fresh ash foliage 

(preferably produced in the field), and small-diameter, 

clean ash logs from sapling trees (either from the field 

or grown in the greenhouse). An adequate supply 

of EAB larvae or adults can sometimes be harvested 

from the field for laboratory use from nearby EAB 

infestations, but laboratory rearing is 

recommended to minimize disease and maximize 

beetle fecundity. Below, we discuss the current bestpractices for mass rearing the emerald ash borer and its 

parasitoids. It should be noted that as new parasitoids 

are introduced, their rearing may also be broadly 

similar to the methods presented here. 

mass rearng emerald ash Borer 

Rearing emerald ash borer in any life stage is time 

consuming. Foliage provided to adult beetles must be 

replaced at least every four days; an efficient system 

for doing so is to maintain two sub-colonies, in which 

insects are given fresh foliage either on Monday and 

Thursday or on Tuesday and Friday. This step requires 

providing the insects with fresh foliage in a clean water 

vial in a fresh, clean container. No additional water 

is necessary, although misting the foliage during the 

provisioning process preserves foliage health. 

Figure 1. Sex determination of emerald ash borer beetles. 

Female is on left; note larger size and wider abdomen, 

especially the two segments just posterior to the hindmost 

pair of legs. Males also have a pronounced silvery pubescence 

(the “beard”) on the ventral surface of the anterior thoracic 

segments. (Photo credit: Jonathan Lelito, USDA APHIS PPQ) 
CHAPTER 8: MASS-REARING OF EAB AND ITS PARASITOIDS

130 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Table 1. Effect of number of females per cage on emerald ash borer fecundity and longevity. 

Number of Females % Enclosures w/Eggs % Producing Mean Total Mean Longevity 

at Initiation 

1 56.8

2 70.2

3 82.0

Optimal rearing of adult beetles, to maximize 

laboratory production of eggs, can be achieved 

using two females and two males (see Fig. 1 for sex 

determination) provisioned with foliage as soon as 

possible following adult eclosion, although a single 

female per cage is also useful for some experimental 

needs (Table 1). Higher numbers of insects per cage 

is not recommended. At least two males should be 

used, regardless of the number of females, to ensure 

mating success (Rutledge and Keena, 2012). Beetles 

are allowed to emerge from field-collected ash logs in 

large cardboard barrels with funnels and jars at one 

end, and the beetles are collected in jars, to which 

beetles are drawn by light (Fig. 2). Alternatively, 

beetles can be reared through their entire life cycle 

in the laboratory in small ash logs (see below). Ash 

leaves used to feed adult beetles must be clean and 

free of pest damage (any decrease in nutrient content 

or increase in plant defense compounds will reduce 

EAB fecundity). The species of ash used as the source 

at 21 d Eggs (d) 

74.6 156 31

78.0 190 37

58.7 96 40

of foliage has significant effects on fecundity, with 

field-collected foliage of mature green ash (Fraxinus 

pennsylvanica Marshall) being the best for massrearing. During the winter, dark green, mature 

foliage from greenhouse-grown tropical ash (Fraxinus 

uhdei [Wenz.] Lingelsh.) can be substituted for green 

ash, but is generally inferior in quality to green 

ash and results in lower beetle fecundity. The EAB 

Rearing Facility in Brighton, Michigan (USA) has 

overcome this problem by having fresh young F. uhdei 

foliage shipped from southern California, where it 

grows as an ornamental. While this source of foliage 

is a more suitable than that from greenhouse-grown 

trees, shipping is expensive when considered over the 

course of a year. 

To house the adult beetle colony, the EAB Rearing 

Facility uses 946 mL clear plastic cups and ventilated 

mesh lids (Fig. 3) such as those available from the 

following source: http://www.joshsfrogs.com/32­

oz-insect-cup-and-lid-placon-cup-250-pack.html. 

Figure 2. Cardboard rearing barrels, with funnels and vials 

inserted into the lids, into which emerald ash borer adults 

collect following their emergence from logs inside barrels. 

This is an efficient system for rearing adult beetles from fieldharvested beetle-infested logs. (Photo credit: Jonathan Lelito, 

USDA APHIS PPQ) 

Figure 3. Emerald ash borer enclosure and setup showing 946 

mL plastic cup, Velcro, water vial with drilled lid (right), and 

ash foliage added (left). This is an appropriate amount of ash 

foliage for 3-4 insects for 3 days. (Photo credit: Jonathan Lelito, 

USDA APHIS PPQ) 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

Figure 4. Emerald ash borer rearing enclosures showing 

screen and filter paper lids secured for oviposition. Tracking 

egg production data is useful for optimizing colony 

demography. A simple data sheet, visible on side of cup, 

records the day of beetle emergence, weekly egg production, 

and the number of beetles dead at each provisioning with 

new foliage. (Photo credit: Jonathan Lelito, USDA APHIS PPQ) 

Inside this plastic cup, a small 5-6 cm diameter disk 

of paper towel is placed on the bottom to absorb 

moisture from frass and foliage. A 3-4 cm strip of 

Velcro (Sticky Back Velcro Tape, 8 m x 1.9 cm, www. 

uline.com) is applied to the inner surface of the 

plastic cup. The matching portion of Velcro is fixed 

to the cap of a 20 mL plastic scintillation vial (Fisher 

Scientific, Product # 03-341-72A). Several 5-7 mm 

diameter holes are drilled into the vial’s cap. The vial 

thus serves as a removable water reservoir to keep 

ash foliage alive while the beetles feed (Fig. 3). Vials, 

fiberglass screens, ventilated mesh lids, and plastic 

cups are bleached after each use. Paper toweling 

and filter paper lids are replaced each time foliage is 

changed. EAB-rearing cages are kept in a walk-in 

growth chamber held at 27 (± 1° C) during the day 

and 22 (± 1° C) at night, with a 16:8 light-dark cycle. 

Relative humidity is held at 75-80 (± 5%). Groups of 

3-4 EAB adults are housed this way for two weeks, at 

which time the type of lid used is changed to facilitate 

egg-laying and collection. The cage construction 

remains the same, but instead of a ventilated lid, a 

10 x 10 cm square of black fiberglass window screen 

is placed on top of the plastic cup. On top of this, 

a single coffee filter paper (Meijer Brand, 8-12 cup 

size) is placed, and both are tightly secured against 

the plastic cup with several small rubber bands. EAB 

Figure 5. Filter paper removed from the top of an emerald ash 

borer-rearing enclosure, showing eggs (brown dots). Number 

of eggs shown is typical production from two emerald ash 

borer females for 3-4 days. (Photo credit: Jonathan Lelito, 

USDA APHIS PPQ) 

adults perceive the fiberglass screening as a rough 

surface under which to deposit eggs (Fig. 4); eggs thus 

laid adhere to the easily removable filter paper, which 

can then be used either to rear egg parasitoids or EAB 

larvae (Fig. 5). 

Egg production and EAB health should be closely 

monitored to ensure rearing success (data sheets on 

the front of cages assist in this effort; Fig. 4). Any 

insects that die should be promptly removed from 

their cages, and any cage that loses more than two 

of the initial four insects should be discarded. Any 

evidence of fungal infection, such as sporulating 

cadavers, must be dealt with swiftly, as outbreaks can 

quickly devastate a large colony. The best methods to 

limit infection and outbreaks are to thoroughly clean 

all supplies, inspect rearing cages before opening to 

prevent transfer of pathogens (e.g., “infected” cages 

are discarded unopened), and remove dead insects 

promptly. Any beetles showing reduced fecundity 

should immediately be isolated. Any rearing cage 

that fails to produce eggs by day 21 post-adult EAB 

eclosion should be discarded even if the beetles 

remain alive – it is likely these insects are of poor 

quality or diseased, as the majority of healthy EAB 

females will lay eggs by this time (Table 1). Egg 

production naturally declines after 9-10 weeks of 

adult life, and to maintain efficiency and limit disease 
CHAPTER 8: MASS-REARING OF EAB AND ITS PARASITOIDS

132 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

Figure 6. An ash log artificially infested with emerald ash 

borer eggs. Small pieces of filter paper bearing beetle eggs 

are secured to the logs, eggs facing inward to facilitate 

establishment of young larvae. (Photo credit: Jonathan Lelito, 

USDA APHIS PPQ) 

all rearing groups should be discarded after this age 

or as soon as egg production begins to decline. 

EAB eggs deposited on coffee filters (Fig. 5) 

provide a convenient means to transfer eggs to ash 

logs, for the production of EAB larvae and pupae. 

EAB eggs can be gently secured to ash logs (Fig. 6) 

using a strip of Parafilm (Fisher Scientific, Cat. No. 

S37440), and inoculated logs then allowed to develop 

in trays of clean water for several weeks (Fig. 7). The 

EAB Rearing Facility uses photographic developing 

trays that are available commercially (Cescolite, Item 

# CL1114T) to maintain logs at this stage. Trays of 

this type are advantageous because excess water can 

be easily poured out, and trays hold a large number 

of ash logs and are highly resistant to chemicals, 

allowing trays to be easily sterilized with bleach after 

use. Larvae serve as hosts for the larval parasitoids 

(see below) or can be allowed to mature and excavate 

pre-pupal cells, after which time they can be used 

for the production of EAB adults. Temperature has 

a significant effect on EAB development and rearing 

temperatures should generally be at or below 30°C for 

optimal development (Duan et al., 2013a), especially 

for adult beetles. A key exception may be the rearing 

EAB larvae at slightly higher temperatures (i.e., 

32-33° C) for more rapid production of larvae to 

serve as hosts for the larval parasitoids (see below). 

At this temperature, mature, 4th instar larvae can be 

produced in about three weeks. 

Figure 7. Emerald ash borer larvae can be reared in freshly cut 

green ash logs (14 cm tall by 5-8 cm wide) held in plastic trays 

(25 x 30 cm) filled with 1-2 cm of clean water. (Photo credit: 

Jonathan Lelito, USDA APHIS PPQ) 

Production of EAB adults using the method 

described above for rearing larvae is advantageous, 

although time consuming. Where wild-collected 

material is available, trees infested with numerous 

EAB can be felled and later warmed for beetle 

emergence in the laboratory. Field-collected material 

is only available seasonally, however, and long-term 

storage (e.g., from winter of the current year until 

the next autumn or winter) severely decreases the 

quality of the insects produced. To avoid these 

problems, EAB-infested ash logs can be incubated at 

warm temperatures for several months to allow full 

larval development, then chilled for several months, 

and later warmed for the production of EAB adults. 

Laboratory-reared adults suffer lower incidence of 

disease and generally have much higher fecundity 

than field-collected EAB adults because the duration 

of cold storage can be precisely controlled. 

mass rearing eaB parasitoids 

Oobius agrili 

Oobius agrili Zhang and Huang (Hymenoptera: 

Encyrtidae), a solitary egg parasitoid of EAB, can 

easily be reared with some modifications of the 

methodology developed by Liu and Bauer (2007). 

All laboratory colonies are parthenogenetic, and 

each female is capable of successfully parasitizing 
CHAPTER 8: MASS-REARING OF EAB AND ITS PARASITOIDS

133 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

at least several dozen EAB eggs in her lifetime (Liu 

and Bauer, 2007). An efficient mass-rearing system 

has been developed using a two-generation system: 

post-diapause O. agrili rearing cages are kept in a 

walk-in growth chamber at 25 (± 1° C), with a 16:8 

light-dark cycle. When provisioned with EAB eggs, 

these insects will produce progeny, a majority of 

which emerge within three to four weeks. Some 

diapausing progeny will be produced under long-day 

conditions (generally around 20% of the total) and 

can be separated by examination under a microscope 

after non-diapausing progeny are allowed to emerge, 

by collecting those parasitized eggs that have no 

exit hole. It is important to note that this process is 

extremely time-consuming in a mass-rearing setting, 

where more than ten thousand EAB eggs must be 

examined per week, and is recommended only if all 

progeny must be collected for specific experimental 

needs. Non-post-diapause O. agrili, produced 

as outlined above, are transferred on the day of 

eclosion to rearing cages kept in a walk-in growth 

chamber held at 25 (±1° C), with an 8:16 light-dark 

cycle. Relative humidity under both photoperiod 

regimes is held at a constant 75-80 (± 5%). The nonpost-diapause individuals, reared under short-day 

conditions, will produce diapausing progeny, which 

can then be stored for up to ten months at 4 ± 1° C 

and high (>75-80%) relative humidity. Storing O. 

agrili in diapause can be done as follows: 21 days 

after first exposure of fresh EAB eggs to adult O. 

agrili, the parasitized eggs are transferred into clean 

cups (i.e., no honey) and moved from 25° C to 10° 

C. After one week at 10° C, parasitized eggs are 

transferred to 4° C until needed. Post-diapause adults 

begin to emerge from cold-stored material after about 

one month of being returned to 25° C, and the cycle 

can be repeated. 

Oobius agrili adults are very small and can easily 

crawl through very small openings, including all 

types of screen tested thus far (even insect netting), 

so care must be taken to maintain proper housing or 

adults will readily escape. Oobius agrili wasps can be 

securely housed in clear plastic 473 mL cups (Gordon 

Food Service, Item # 7922500) fitted with very tight, 

solid clear-plastic lids (Solo Brand, Item # 626TP0090). Lids can be re-used, but must be assessed for 

a

b

c

Figure 8. Emerald ash borer eggs at various stages of 

development. (a) freshly laid, suitable for oviposition of 

Oobius agrili; (b) 24-36 hours old, suitable for oviposition by 

Oobius agrili; (c) upper egg deflated and perhaps damaged; 

lower egg 2-3 days old and less likely to be parasitized unless 

presented immediately. (Photo credit: Jonathan Lelito, USDA 

APHIS PPQ) 

tight fit – if the lid is used many times, it can become 

deformed and this may allow insects to escape. 

Nutrition must be provided to the wasps to ensure a 

normal life span of 2-3 weeks and optimal progeny 

production. Honey can be streaked directly onto 

the interior walls of the plastic cup using a very fine 

tool, such as a single hair from a brush. Care must 

be taken to ensure that the streaks are fine (<0.25 

mm) so that the wasps do not become trapped as they 

attempt to feed. The relative humidity in the rearing 

environment will cause the honey streaks to absorb 

moisture, and this will provide O. agrili adults with 

sufficient water. No more than 5-6 streaks are needed 

per enclosure for a 1-wk period. 

Healthy EAB eggs, deposited on filter papers (Fig. 

5), can be provided to O. agrili females beginning 

on the day of their emergence. Groups of up to 20 

females can be held together in a single 16 oz. plastic 

cup, stocked with fresh EAB eggs once per week 

at a rate of 3-5 EAB eggs per O. agrili female. This 

generally results in parasitism rates of greater than 

75%. Lower rates commonly result from using older 

EAB eggs (>3-4 days post-harvest), many of which 

will develop to near hatching during the course of 

exposure to O. agrili adults and will not be parasitized 

(Fig. 8). Groups of O. agrili adults in which no 

significant mortality has occurred, can be re-used 

for an additional week by moving them to a new, 
CHAPTER 8: MASS-REARING OF EAB AND ITS PARASITOIDS

134 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

 

Figure 9. Supplies needed for creation of larval-bolt exposures 

for rearing emerald ash borer larval parasitoids. Clockwise 

from upper left: completed exposure cage with honey, empty 

cup with floral foam disk, sliced rectangle and circle cut with 

masking tape roll, floral foam brick and EAB-infested ash log 

(center). (Photo credit: Jonathan Lelito, USDA APHIS PPQ) 

clean cup freshly streaked with honey, to which the 

appropriate number of EAB eggs have been added. 

Transferring O. agrili adults between cups is best 

accomplished by removing all other material from 

the cup (filter papers, dead wasps, and hatched EAB 

larvae), and then simply tapping the live wasps into 

the new cup. Fecundity decreases rapidly in groups 

of females more than two weeks of age and re-using 

adults for a third exposure is not recommended. 

Spathius agrili 

Spathius agrili Yang (Hymenoptera: Braconidae) is 

a gregarious idiobiont larval ectoparasitoid of EAB. 

Adult females are robust, capable of living for several 

months, and able to produce several dozen progeny 

during this time (Gould et al., 2011). At 25-27° C, 

one month is required from adult emergence to the 

production of new adults. New adult females need to 

be separated into groups of not more than 20-25 soon 

after emergence to prevent mortality from crowding. 

Spathius agrili can be easily housed in the same 473 

mL cups as O. agrili, with the modification of using 

insect netting (www.skeeta.com, 625 holes per sq. in.) 

secured over the opening of the cup with a rubber 

band, rather than a solid lid. Honey is streaked into 

this screen (and replaced as it is consumed) and 

wasps are misted daily with clean, reverse osmosis 

water. 

Figure 10. Groups of Spathius agrili females are more efficient 

at parasitism and progeny production than single individuals. 

Several females often aggregate over unparasitized hosts; after 

parasitism occurs by one or more (often several) individuals, the 

group disperses and reforms over the gallery of another host. 

(Photo credit: Jonathan Lelito, USDA APHIS PPQ) 

To mass rear S. agrili (and Tetrastichus 

planipennisi Yang as well, see below), EAB larvae are 

reared in small-diameter ash bolts in the laboratory 

until they reach the appropriate stage, and then hostinfested logs are exposed to groups of adult wasps. 

Using a simple set of supplies (Fig. 9), EAB-infested 

ash logs can be exposed to parasitoids. The same 946 

mL cups used to hold adult EAB beetles can be used 

here too, with minor modifications. Instead of a pad 

of paper towels, a disk of floral foam is added to the 

bottom of the cup to retain moisture. Floral foam 

bricks (http://www.save-on-crafts.com/artesia.html) 

are sliced into thin (4-6 mm) rectangular sections 

using a sharp knife. The inner cardboard circle from a 

roll of masking tape can be used as a circular “knife” 

to cut disks of floral foam from these rectangular 

slices; disks are then placed in the bottom of the 

plastic cups. The EAB-infested ash log is then firmly 

pushed into the floral foam, and clean water added 

until the foam is saturated. Wasps are added using an 

electric aspirator, a piece of insect netting is secured 

over the opening of the cup with a rubber band, 

and the netting is streaked with honey to provide 

nutrition to the adult wasps (Fig. 9). The setup is 

then held at 25-27° C and 75-80% relative humidity, 

under a 16:8 light-dark cycle, for one week. After this 

incubation period, the adult wasps can be removed 

with an aspirator and re-used in another exposure. 

The parasitoid-exposed log is then incubated under 
CHAPTER 8: MASS-REARING OF EAB AND ITS PARASITOIDS

135 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

the same conditions, and adults emerge in 2-3 weeks. 

Using the methods outlined above (see section on 

EAB) to produce ash bolts bearing EAB larvae, logs 

set up to rear EAB should be exposed to parasitoids 

between days 24 and 26 post-setup, to ensure that the 

larval hosts have achieved the greatest possible mass, 

and yet have not burrowed into the xylem, where 

they are inaccessible to the parasitoids. Each rearing 

cage should be stocked with 10 S. agrili females and 

2-3 males and an EAB-infested ash log. This group 

of wasps can be used for up to three additional 1-wk 

exposures to fresh EAB-infested ash logs. Groups of 

females often form oviposition aggregations and a 

group size of 8-10 is best to facilitate rapid parasitism 

of most hosts in a container (Fig. 10). Groups with 

moderate mortality (2-3 dead females) during their 

second and third exposures to hosts can generally 

be re-used, combining wasps as necessary to keep 

group size in the optimal range, provided no signs of 

disease, such as sporulating cadavers, are present. If 

any evidence of disease is detected, all wasps in the 

affected group should be discarded. 

To store S. agrili during the winter, diapause 

can be induced during the wasp’s larval stage by 

manipulating temperature and photoperiod (Belill 

and Lelito, 2011). However, emergence from 

diapause occurs over several months and is relatively 

unpredictable. Holding some wasps in diapause (at 

immature stages) is, therefore, not particularly useful 

for mass-rearing since production cannot be well 

enough timed to produce synchronized groups of 

parasitoids for release. The method does have some 

value for storing field-collected material for long 

periods and for limiting the number of generations 

that a colony is subjected to laboratory rearing. Adults 

from cocoons (containing mature larvae) stored 

under cold conditions for several months have lower 

fecundity and higher mortality (Gould et al., 2011). 

Methods for storing S. agrili that bypass the need for 

diapause are still under development. 

Spathius galinae 

Spathius galinae Belokobylskij & Strazanac 

(Hymenoptera: Braconidae) is a recently described 

EAB parasitoid from the Russian Far East and South 

Korea (Belokobylskij et al., 2012). It was imported to 

Figure 11. Exposure arena for production of Spathius galinae, 

containing five gravid female parasitoids and five males, as 

well as tropical ash logs infested with late instars of emerald 

ash borer. (Photo by Timothy Watt and Jian Duan (USDA ARS 

BIIR)) 

the USDA ARS Beneficial Insects Quarantine Facility 

(Newark, Delaware) in 2010 and its host range has 

been studied to estimate the safety of its release 

in the United States against the emerald ash borer 

(Gould and Duan, 2013). A petition for field release 

of S. galinae was submitted to the USDA APHIS and 

NAPPO in March of 2013 for regulatory review and 

approval. While not yet (January, 2015) approved 

for field-release, a positive response from NAPPO 

and USDA APHIS has been issued to the petition’s 

scientists and the parasitoid’s potential future massrearing is described here. Based on its distribution in 

the Russian Far East and other part of northeast Asia, 

climatic matching suggests that it is more suitable 

for introduction against emerald ash borers in the 

northeast United States and Canada (Duan et al., 

2012; Gould and Duan, 2013) than the previously 

introduced Chinese parasitoids (e.g., Liu and Bauer, 

2007; USDA APHIS, 2007). 

Specific rearing methods have recently been 

developed at the USDA ARS Beneficial Insects 

Research Unit. The first step is the exposure of mated 

female wasps to 3rd-4th instars EAB larvae naturally 

reared on freshly cut green or tropical ash logs (Fig. 

11). Spathius galinae takes about one month (29 d) 
CHAPTER 8: MASS-REARING OF EAB AND ITS PARASITOIDS

136 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

to complete a generation (from egg to adult) under 

laboratory conditions (25 ± 1° C, 65 ±10% RH, L:D 

16:8 h photoperiod). During this period, S. galinae 

larvae molt four times to reach the 5th instar, which 

then spins a cocoon for pupation and development 

to the adult stage. Adult female wasps survive 

seven weeks on average, with the peak oviposition 

occurring after three weeks when wasps are reared in 

groups, or after two weeks when wasps are reared as 

single pairs. Throughout its lifespan, one S. galinae 

female produces an average of 31 progeny (range 12­

41) when reared in groups, but many more offspring 

(ave. 47, range 5-94) when reared as single pairs. 

Thus, in mass rearing S. galinae, adult wasps can 

be exposed to hosts for several weeks. Although S. 

galinae can be reared in emerald ash borer larvae in 

either green or tropical ash sticks, the rate of nonemergence of S. galinae progeny was much higher 

(20%) when wasps were reared on hosts in green ash 

sticks than in tropical ash sticks (2.1%). 

Temperatures below 15o C induce mature S. 

galinae larvae (inside cocoons) to enter an obligatory 

diapause. Once in diapause, a minimum of 1-3 

months of chill at 3-12o C is required to break 

diapause and permit development to the adult stage. 

Specific mechanisms that induce and break diapause 

for this species are still being investigated. Unlike S. 

agrili, we have found that material can be stored up 

to six months with no decrease in adult emergence; 

however, it is not known if cold storage affects fitness 

or performance of adults. 

Tetrastichus planipennisi 

Tetrastichus planipennisi (Hymenoptera: Eulophidae) 

is a gregarious koinobiont larval endoparasitoid 

of EAB. The rearing method for T. planipennisi is 

similar to that for S. agrili, with a few key differences. 

First, rearing logs used should be from smaller trees 

whose bark is not more than 3 mm thick (Ulyshen et 

al., 2010; Abell et al., 2012). Second, the number of 

parasitoid adults per exposure cage should be slightly 

larger (12-15) than that used for S. agrili. Third, ash 

logs used to rear EAB larvae should be exposed to 

T. planipennisi a few days earlier (22-24 days postsetup of the EAB rearing) than for S. agrili to ensure 

Figure 12. When nearly mature, the larvae of Tetrastichus 

planipennisi confer a braided appearance on their host 

larva. At this point or just afterwards, T. planipennisi broods 

can be induced into a state of torpor and be stored at low 

temperatures for up to six months without significant 

mortality. (Photo credit: Jonathan Lelito, USDA APHIS PPQ) 

that the wasps have time to locate and parasitize 

all available EAB. Finally, groups of T. planipennisi 

females should only be used twice, as further use 

results in fewer progeny. Rearing of T. planipennisi is 

optimal at 25° C, 75-80% relative humidity, and a 16:8 

light-dark cycle. Honey should be available to insects 

at all times, streaked on lids of rearing containers. 

Another key difference between T. planipennisi 

and S. agrili is that T. planipennisi can be induced 

into a torpor state late in larval development, and in 

this condition T. planipennisi can be stored for long 

periods at 4 (±1° C) provided relative humidity is 

>75-80%. To induce torpor, immature parasitoids are 

chilled to 10° C on day 14 after host exposure to adult 

wasps, which is approximately when T. planipennisi 

larvae break out of their host larvae (Fig. 12). Logs 

can be held on moist floral foam in the rearing cages 

or they can be transferred into trays of shallow, 

clean water. Seven days after being placed at 10° 

C, rearing logs are transferred (remaining on moist 

foam or in shallow, clean water) to 4° C for storage. 

Mortality is generally <10% of the total cohort in 

each log when stored for up to six months. Under 

these conditions, most deaths are caused by bark 

drying and contracting, which crushes or traps some 

insects. Independent of bark desiccation, mortality 

increases during storage, as insects deplete metabolic 

reserves. Following return of stored wasps to 25° C, 
CHAPTER 8: MASS-REARING OF EAB AND ITS PARASITOIDS

137 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

T. planipennisi adults will usually emerge within 14 

days, although some emergence may occur through 

day 21. Thus, unlike diapausing S. agrili, larvae of T. 

planipennisi can be stored in a manner that allows 

emergence of wasps to be predicted and controlled. 

reFerenCes 

Abell, K., J. Duan, L. Bauer, J. Lelito, and R. Van 

Driesche. 2012. The effect of bark thickness 

on host partitioning between Tetrastichus 

planipennisi (Hymen: Eulophidae) and Atanycolus 

spp. (Hymen: Braconidae), two parasitoids 

of emerald ash borer (Coleop: Buprestidae). 

Biological Control 63: 320-325. 

Belill, V. and J. P. Lelito. 2011. Understanding 

diapause in Spathius agrili – the roles of 

photoperiod and temperature, pp. 103-104. In: 

Parra, G., D. Lance, V. Mastro, R. Reardon, C. 

Benedict (Compilers). Proceedings of the 2011 

Emerald Ash Borer National Technology and 

Research Development Meeting. 12-13 October, 

2011. Wooster, Ohio. USDA Forest Service, 

FHTET-2011-06, Morgantown, West Virginia, 

USA. 

Belokobylskij, S. A., G. I. Yurchenko, J. S. Strazanac, 

A. Zaldívar-Riverón, and V. Mastro. 2012. 


A new emerald ash borer (Coleoptera: 


Buprestidae) parasitoid species of Spathius Nees 


(Hymenoptera: Braconidae: Doryctinae) from the 


Russian Far East and South Korea. Annals of the 


Entomological Society of America 105: 165-178. 


Duan, J., G. Yurchenko, and R. Fuester. 2012. 

Occurrence of emerald ash borer and biotic 

factors affecting its immature stages in the 

Russian Far East. Environmental Entomology 41: 

245-254. 

Duan, J., T. Watt, P. Taylor, K. Larson, and J. P. Lelito. 

2013a. Effects of ambient temperature on egg and 

larval development of the invasive emerald ash 

borer (Coleoptera: Buprestidae): Implications 

for laboratory rearing. Journal of Economic 

Entomology 106: 2101-2108. 

Duan, J. J., K. Larson, T. Watt, J. Gould, and J. P. 

Lelito. 2013b. Effects of host plant and larval 

density on intraspecific competition in larvae of 

the emerald ash borer (Coleoptera: Buprestidae). 

Environmental Entomology 42: 1193-1200. 

Gould J. R. and J. J. Duan. 2013. Petition for 

release of an exotic parasitoid, Spathius galinae 

Belokobylskij & Strazanac, for the biological 

control of the emerald ash borer, Agrilus 

planipennis Fairmaire.  USDA APHIS Petition 

2013-01. 

Gould, J., T. Ayer, and I. Fraser. 2011. Effects of 

rearing conditions on reproduction of Spathius 

agrili (Hymenoptera: Braconidae), a parasitoid of 

the emerald ash borer (Coleoptera: Buprestidae). 

Journal of Economic Entomology 104: 379-387. 

Liu, H. and L. Bauer. 2007. Oobius agrili 

(Hymenoptera: Encyrtidae), a solitary egg 

parasitoid of emerald ash borer from China, 

pp. 63-64. In: Mastro, V., D. Lance, R. Reardon, 

and G. Parra (compilers). 2006. Emerald Ash 

Borer and Asian Longhorned Beetle Research and 

Development Review Meeting, Cincinnati, Ohio. 

USDA FS FHTET-2007-04, Morgantown, West 

Virginia, USA. http://nrs.fs.fed.us/pubs/9566 

Rutledge, C. and M. Keena, M. 2012. Mating 

frequency and fecundity in the emerald ash borer, 

Agrilus planipennis (Coleoptera: Buprestidae). 

Annals of the Entomological Society of America 

105: 66-72. 

Ulyshen, M., J. Duan, L. Bauer, and I. Fraser. 2010. 

Suitability and accessibility of immature Agrilus 

planipennis (Coleoptera: Buprestidae) stages 

to Tetrastichus planipennisi (Hymenoptera: 

Eulophidae). Journal of Economic Entomology 

103: 1080-1085. 

USDA APHIS. 	2007. The proposed release of 

three parasitoids for the biological control of 

the emerald ash borer (Agrilus planipennis) in 

the continental United States: environmental 

assessment. Federal Register 72: 28947 – 28948, 

Docket No. APHIS-2007-006. 

139 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Chapter 9: liFe taBle evalUation oF Change in emerald ash Borer popUlations 

dUe to BiologiCal Control 

David E. Jennings1, Jian J. Duan2, Kristopher J. Abell3, Leah S. Bauer4, 


Juli R. Gould5, Paula M. Shrewsbury1, and Roy G. Van Driesche3
 

1

Department of Entomology, University of Maryland, College Park, Maryland 20742
 

2

USDA, Agricultural Research Service, Beneficial Insects Introduction and Research Unit, Newark, Delaware 19731
 

3

Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts 01003
 

4

USDA, Forest Service, Northern Research Station, East Lansing, Michigan 48823
 

5

USDA, APHIS PPQ, Center for Plant Health Science and Technology, Buzzards Bay, Massachusetts 02542
 

BaCKgroUnd 

Emerald ash borer, Agrilus planipennis Fairmaire 

(EAB), is an invasive buprestid native to northeastern 

Asia that feeds on ash trees (Fraxinus spp.). First 

detected in North America (in Michigan, United 

States and Ontario, Canada) in 2002, EAB has spread 

rapidly, in part because of movement of infested 

nursery stock and untreated firewood (Cappaert et al., 

2005a; BenDor et al., 2006; Poland and McCullough, 

2006). As of January 2014, EAB was known in an 

additional 21 U.S. states and one Canadian province 

(USDA-APHIS, 2014), and it is expected to continue 

spreading to other parts of the continent with ash 

trees and a suitable climate (Sobek-Swant et al., 

2012; Vermunt et al., 2012; DeSantis et al., 2013). 

Thus far, EAB has killed tens of millions of ash 

trees, with tree death generally occurring within 3-4 

years of initial infestation by the beetle (Poland and 

McCullough, 2006). The treatment, or removal and 

replacement of landscape trees affected by this pest is 

projected to cost over $10 billion in the United States 

in the coming decade (Kovacs et al., 2010). While 

insecticide treatments can be effective at reducing 

losses from EAB in urban settings, biological control 

might represent the most sustainable option for 

suppressing populations at the landscape level and in 

natural environments over the long term. 

The primary risk factor for North American ash 

is their limited innate host resistance to EAB (Liu et 

al., 2003; Bauer et al., 2005; Gould et al., 2005; Rebek 

et al., 2008; Herms and McCullough, 2014). Another 

cause of high ash mortality in North America is 

the lack of host-specific EAB natural enemies. In 

EAB’s native range, however, parasitoids cause a 

considerable proportion of EAB egg and larval 

mortality, potentially regulating host population 

densities (Liu et al., 2003, 2007; Bauer and Liu, 2007; 

Wang et al., 2010; Duan et al., 2012a). In 2007, the 

USDA started the EAB Biological Control Program 

(Federal Register, 2007; Bauer et al., 2008), and 

began releasing three EAB parasitoids from China 

in the United States. These biological control agents 

are the larval ectoparasitoid Spathius agrili Yang 

(Yang et al., 2005, 2010), the larval endoparasitoid 

Tetrastichus planipennisi Yang (Liu et al., 2003, 2007; 

Yang et al. 2006; Duan et al., 2011a), and the egg 

parasitoid Oobius agrili Zhang and Huang (Zhang et 

al., 2005; Liu et al., 2007; Duan et al., 2011b; Duan 

et al., 2012b). Understanding the basic population 

dynamics of EAB will enable us to assess the effects 

of parasitism on EAB population growth and to more 

effectively target different life stages with biological 

control agents. One widely used approach to 

examining population dynamics is through life table 

analysis. Here, we briefly introduce some of the basic 

concepts of life tables, and then review some of the 

methods and results from life table analyses involving 

EAB. 

liFe taBles 

Life tables are constructed from data on the numbers 

of individuals that enter or die in different age or 

stage classes of populations over the course of a 
CHAPTER 9: LIFE TABLE EVALUATION OF CHANGE IN EAB POPULATIONS DUE TO BIOLOGICAL CONTROL

BIOLOGY AND CONTROL OF EMERALD ASH BORER

generation (Van Driesche and Bellows, 1996; Stiling, 

2012). Life tables have been used in ecology for over 

65 years (Deevey, 1947), and they have provided 

insight into the population dynamics of a range of 

taxa including plants (Harcombe, 1987), fish (Cortes, 

2002), mammals (Sherman and Morton, 1984), reptiles 

(Crouse et al., 1987), and insects (Hawkins et al., 

1997). Early work in this field involved constructing 

life tables for the winter moth (Operophtera brumata 

L.) (Lepid.: Geometridae) (Varley and Gradwell, 1960; 

Buckner, 1969), and life tables have subsequently been 

employed widely in applied entomology for assessing 

the impact of pest control measures (Gould et al., 1992; 

Hoddle and Van Driesche, 1999; Kuhar et al., 2002; 

Nielsen et al., 2008). These effects can be examined 

either experimentally by manipulating certain sources 

of mortality in the field, or by modelling population 

dynamics with and without factors of interest in the 

model. For a more detailed discussion of life tables in 

general see Bellows et al. (1992) or Southwood and 

Henderson (2000). 

Types of Life Tables 

Two main types of life tables are utilized used in 

ecology: horizontal (cohort) and vertical (static) 

life tables (Van Driesche and Bellows, 1996; Stiling, 

2012). Horizontal life tables follow a given cohort 

of same-aged individuals from birth throughout 

their lives, while vertical life tables use data from a 

population at one particular point in time. Vertical 

life tables often are used when study organisms are 

long-lived and it is not practical to follow them 

throughout their lives, and vertical life tables are 

Table 1. Life table for an experimentally established EAB cohort at Legg and Central Parks, Meridian Township, Michigan in 2010. 

Life stage 1 x m x d x di Mortality factor qx qi q 

(egg) 229 0 69 Infertility/predation/parasitism by Oobius agrili 0.300 0.300 0.300 

L1-L2 160 0 34 34 Killed by tree resistance 0.213 0.557 0.149 

L3 126 0 22 15 Killed by tree resistance 0.175 0.119 0.066 

3 Undetermined disease/other 0.024 0.013 

4 Parasitism (Atanycolus spp.) 0.068 0.018 

L4 104 1 32 4 Undetermined disease/other 0.308 0.038 0.018 

7 Killed by tree resistance 0.067 0.031 

18 Parasitism (Atanycolus spp.) 0.173 0.079 

1 Parasitism (Balcha indica) 0.010 0.004 

2 Woodpecker predation 0.019 0.009 

JL 71 9 52 52 Woodpecker predation 0.732 0.732 0.228 

Adult exit hole 10 9 1 1 Undetermined disease/other 0.000 0.100 0.004 

observed 

(Overwintered 

L4/JL-pupae) 

10 - 3 3 29% additional overwintering woodpecker 

predation 

0.290 0.290 0.013 

(Emerging 

adults) 

16 - 1 1 5% adult mortality from disease and predation 0.050 0.050 0.004 

(Females) 8 - - 1:1 sex ratio 

(F1

 eggs) 812 - - 101.5 eggs per female 

R0 3.6 - -

140 
CHAPTER 9: LIFE TABLE EVALUATION OF CHANGE IN EAB POPULATIONS DUE TO BIOLOGICAL CONTROL

141 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

more suited for continuously breeding organisms 

with overlapping generations. Either method may 

be used for EAB, but given that we are able to create 

experimental cohorts of larvae, the horizontal (or 

stage-specific) life table may be more suitable. 

Life Table Parameters 

Several different parameters are used in life tables, 

and here we follow the general methods and column 

definitions described in Southwood and Henderson (2000). Table 1 is presented as an example of a 

stage-specific life table for EAB constructed from 

data collected in Michigan. Column headings are lx 

= number of live EAB entering each stage (based on 

reverse calculation of the different stages of EAB observed at the sampling time, and with l0

 representing 

the number of eggs estimated to start the life table); 

mx

 = number of live EAB observed at sampling time, 

dx

 = number of dead EAB observed in each stage; qx 

= apparent (stage-specific) mortality rate (dx/lx); di = 

number of EAB dying in association with the specific 

factor observed, qi

 = apparent mortality rate because 

of the specific biotic factor di/lx); q = real mortality 

(dx

 or di/l0), R0 = net reproductive rate, calculated as 

the ratio of l0

 divided by lF1 (the number of eggs produced by surviving adults). R0

 can be interpreted as 

follows: if R0

 = 1, the population is constant; if R0 > 1, 

the population is growing; and R0

 < 1, the population 

is declining. 

Apparent Mortality 

Expressing the number of individuals dying in a stage 

as a percentage of the number entering the stage 

generates the estimate of apparent mortality (Van 

Driesche and Bellows, 1996). Apparent mortality can 

subsequently be used to calculate k-values, as k = 

-log(1 – apparent mortality). Apparent mortality is 

generally used to estimate a single source of mortality 

within an individual life table, while k-values are 

additive over several mortality factors within a given 

life table and can be used to identify the key mortality 

factor for a population if life tables are available for a 

series of generations. 

Marginal Attack Rates 

For situations in which there are multiple contemporaneously acting mortality factors (e.g., predators 

consuming prey, some of which have already been 

parasitized), calculating the marginal attack rate is an 

improvement over apparent mortality (Elkinton et 

al., 1992). A marginal attack rate is the proportion of 

individuals entering a stage that are subject to attack 

by a given factor (A), even if some other factor (B) 

ends up actually killing some individuals previously 

attacked by factor A. It can be calculated using the 

following equation: mi

 = 1 – (1 – d)di/d . This may be 

especially important with EAB because it is likely that 

some EAB larvae are stung by parasitoids but later 

consumed by woodpeckers or other insectivorous 

birds before immature parasitoids complete their 

development and kill their host. 

ConstrUCting liFe taBles For eaB 

EAB Life Cycle 

Constructing life tables for EAB requires detailed 

knowledge of the species’ life cycle (see Chapter 

1). EAB females generally produce about 100 eggs 

(Wei et al., 2007; Wang et al., 2010), which are laid 

underneath small bark flakes or in crevices on ash 

trees. In Michigan, EAB’s peak oviposition period 

occurs during late spring through summer (Poland 

and McCullough, 2006), and this appears to be the 

case throughout most of its North American range. 

Upon hatching, larvae burrow into the cambium 

and feed on the phloem and outer sapwood. Larvae 

develop through four instars in summer and fall, 

form a pupal chamber or cell (see Chapter 1), and 

overwinter in an obligatory diapause as mature 4th 

instar larvae. Under some circumstances, larvae 

require two years to complete development (Cappaert 

et al., 2005a,b) (see further discussion of this below). 

Adults begin emerging from ash trees in late spring or 

early summer (Brown-Rytlewski and Wilson, 2005) 

and feed on ash foliage throughout their lives. EAB 

adults mate within days of emerging, and oviposition 

typically begins after another week or two depending 
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142 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

on weather conditions (Cappaert et al., 2005a). 

Given the cryptic nature of wood-boring insects, 

the life cycles of beetles such as EAB present many 

challenges for the construction of life tables. For 

instance, because EAB’s eggs are laid between layers 

of bark and in bark crevices, they are not easily 

counted by observers. Furthermore, the majority 

of the EAB life cycle takes place as larvae feed, 

develop, and pupate inside host trees. This effectively 

prohibits repeated sampling as larval fates can only be 

determined by debarking trees, making it impossible 

to determine exactly when individuals might have 

died (although using stage-specific life tables can 

circumvent this). Additionally, wild EAB populations 

can be either univoltine (one-year generation 

time) or semivoltine (multi-year generation time), 

which appears to be influenced by climate, host 

tree condition, and oviposition date (Cappaert 

et al., 2005a,b). Having populations with mixed 

generations presents problems because individuals 

may not be exposed to a specific mortality factor for 

the same length of time or during the same season. 

For example, semivoltine larvae developing over two 

growing seasons will have a longer period of exposure 

to parasitoids than univoltine larvae that complete 

develop after one growing season. 

Life table analyses for EAB have been conducted 

in Maryland, Michigan, and New York. In Michigan, 

a life table approach was used to assess the 

effectiveness of biological control agents released over 

three generations of EAB (Duan et al., 2010; Duan 

et al., 2014). In Maryland and New York, a life table 

approach was used by Jennings et al. (2013), primarily 

to explore the effect of woodpecker predation on EAB 

populations, although parasitism rates from biological 

control agents were also quantified. 

Establishing Experimental Cohorts 

Several methods have been created to establish 

experimental cohorts of EAB in ash trees, which 

subsequently enabled accurate quantification of 

their population dynamics. For example, Duan et al. 

(2010) used two methods to establish EAB cohorts in 

Michigan. Their first method involved the placement 

of laboratory-reared EAB eggs directly onto the tree. 

To achieve this, EAB adults were first induced to 

lay eggs underneath strips of ribbon on small ash 

logs in the laboratory (the ribbon simulating loose 

bark crevices found naturally on ash trees). Using a 

utility knife, small bark flakes (to which at least one 

egg was attached) were then cut from the logs and 

taken to the field. Bark flakes were inserted under 

bark flaps cut into ash trunks with knives, and the 

flaps were then pinned to the tree to offer protection 

from predators but still allow enough space so as not 

to crush the eggs. This method is labor intensive as 

it requires the production of eggs in the laboratory, 

and resulted in rates of EAB larval establishment of 

14-26% (Duan et al., 2010). On the positive side, this 

method may retain some of the contact pheromones 

from EAB females, and it allows for placement of 

precise numbers of eggs in the field. 

The second method utilized by Duan et al. (2010) 

was to cage gravid EAB females on trees (along with 

males and ash leaves), which forced oviposition to 

occur within a specific region of the tree. Cages were 

constructed from ventilated, rectangular containers 

(10 cm long x 7 cm wide x 4 cm deep) that were 

fastened to the trees, with the open side facing the 

trunk. One female and one male were placed into 

each cage. Benefits of this method were that it again 

allows for the retention of any contact pheromones 

from adult beetles, and it allows EAB females to 

oviposit naturally onto the bark. This method resulted 

in a higher rate of establishment in comparison with 

insertion of eggs into bark flaps, with ~75% of eggs 

producing established larvae (Duan et al., 2010). 

This method can be problematic, however, because 

quantifying the exact number of eggs produced 

is challenging, as some eggs may be overlooked 

or damaged during sampling via debarking. 

Furthermore, because of the variation in the number 

of eggs produced by females and consequently in 

larval density, statistical comparisons among trees can 

be difficult. 

A third method, used by Jennings et al. (2013), 

modified the approach from Duan et al. (2010) 

that involved grafting individual EAB eggs directly 

onto the tree (Abell et al., 2012). For this method, 

eggs were first laid on a coffee filter paper substrate 

by EAB females in the laboratory. Strips of filter 

paper containing 1-3 fertilized eggs (as indicated by 
CHAPTER 9: LIFE TABLE EVALUATION OF CHANGE IN EAB POPULATIONS DUE TO BIOLOGICAL CONTROL

143 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

a b c d

Figure 1. Method for establishing experimental cohorts of EAB on ash trees. Shown are: (a) attaching eggs to bark, (b) covering 

eggs with cotton balls, (c) protecting eggs further with tree wrap, and (d) repeating on tree as desired, ensuring that bands of 

eggs are evenly distributed to avoid overlapping galleries (Photo credit: David Jennings, University of Maryland) 

brownish color) were then cut and transported to 

field sites. Once suitable trees were identified at field 

sites, small patches of bark were shaved flat using a 

draw knife. Egg strips were then glued flush to the 

bark using standard wood glue, taking care to ensure 

that no glue came into contact with the eggs (Fig. 

1a). To reduce the chances of galleries overlapping, 

a maximum of three eggs were placed on any one 

bark patch. Once the egg strip had been attached, 

a cotton ball was glued over the eggs, to reduce the 

risk of predation (Fig. 1b). This was replicated until 

there were six eggs at a particular height on the tree (a 

“band”). Once a band was completely inoculated with 

eggs, it was covered in tree wrap to limit predation 

(Fig. 1c). This process was repeated until there were 

five bands, each containing six eggs, on the tree for 

a total of 30 eggs (Fig. 1d). This method allows for 

a more precise number of eggs to be deposited on 

each experimental tree section. However, it appears 

to lower the rate of eggs transferring into established 

larvae, with estimates of establishment being ~54% 

(Jennings et al., 2013). Producing the eggs for this 

method is also labor intensive as it again requires 

the production of eggs in the laboratory, and care 

is needed when cutting the filter paper into strips. 

Additionally, this method precludes predation on the 

eggs themselves, removing this mortality factor from 

the life table. However, anecdotal evidence suggests 

that use of uncovered egg strips results in extremely 

high egg mortality, likely from predation. 

Wild Populations 

Life tables can also be constructed by directly 

sampling survival of life stages in wild populations 

of EAB (Jennings et al., 2013; Duan et al., 2014) by 

debarking sections of the tree and following the same 

process for identifying sources of mortality as with the 

experimental populations described above. However, 

several key caveats must be acknowledged when using 

wild populations for life table construction. The most 

obvious is that it is not possible to be certain how 

many eggs were laid on a tree in that year, given the 

difficulty associated with locating every egg on a tree 

and dating them. One approach to provide an estimate 

of the number of eggs per tree could be to search a 

given area of a tree and then extrapolate those findings 

for the rest of the tree. Additionally, it is not possible to 

state with certainty whether populations being studied 

are univoltine or semivoltine. The latter is strongly 

suggested if debarking of trees in the fall reveals many 

early instar larvae (likely being young of the sample 

year, whereas older larvae would have originated in 

the previous year and hence belong to a different 

generation). Despite these problems, constructing 

life tables for EAB in heavily infested areas can still 

provide valuable information on population dynamics. 

At such areas, it might not be possible to determine 

the fate of experimental cohorts given the high density 

of other galleries, and monitoring wild populations 

may be the most effective option at present. 
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144 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Assigning Individuals to EAB Life Stages 

Eggs. EAB eggs are around 1 mm in diameter 

and change color from white to brown a few days 

after being laid (Bauer et al., 2004; Wang et al., 2010). 

Such eggs found between layers of ash bark are 

presumed to be those of EAB. 

Larvae and pupae. EAB larvae create 

characteristic serpentine galleries (Bauer et al., 

2004; Lyons et al., 2004). Because the gallery size 

of EAB larvae changes over time, it can be used to 

estimate the stage the larva was in when it died, 

for example <2 mm wide for 1st to 2nd instars, 2-3 

mm wide for 3rd instars, and >3-4 mm wide for 

4th instars. Larvae then chew a pupation chamber 

in the outer sapwood or bark before folding into a 

J-shape for overwintering. These mature 4th instar 

larvae are termed J-larvae (Duan et al., 2010), but are 

sometimes referred to as prepupae (Chamorro et al., 

2012) (see Chapter 1 for clarification). 

Adults. For the purposes of life tables, EAB can 

be assigned as adults if there is evidence that they 

have successfully emerged from their pupal chamber, 

as indicated by a D-shaped exit hole in the bark. 

Adults are generally <10-13 mm in size and bright 

metallic green in color, and can live for 3-6 weeks 

after emergence (Cappaert et al., 2005a; Parsons, 

2008). 

Estimating Fecundity 

Estimating fecundity from experimentally established 

cohorts or wild populations is extremely difficult, and 

thus far EAB life table studies have used fecundity 

data collected from laboratory-reared females. 

However, one problem with using estimates from 

laboratory-reared females is the high variation in 

the number of eggs produced. While some estimates 

have suggested that EAB females produce about 100 

eggs (Wei et al., 2007; Wang et al., 2010), other data 

from laboratory-reared EAB showed an average of 74 

eggs (range of 1 to 307 eggs per female (EPPO, 2013). 

Given the optimal rearing conditions in laboratories, 

it is possible that these are overestimates compared 

to field conditions. Alternatively, when logistically 

possible, sections of trees where EAB cohorts have 

been placed could be caged to trap and collect 

emerging adults. These adults could then be reared in 

the laboratory to obtain direct estimates of fecundity. 

However, cages would need to be checked frequently 

to minimize adult mortality. 

Assigning Deaths in EAB Life Stages to 

Particular Mortality Factors 

Eggs. Several methods have been developed to 

assess egg mortality under field conditions. One 

simple method involves searching for EAB eggs 

between thin layers of bark, typically for a set period 

of time, which then avoids problems associated with 

tree size (Duan et al., 2011b; Bauer et al., 2012; Duan 

et al., 2012b). Alternatively, estimates of egg mortality 

can be obtained through the use of egg sentinel logs 

(ESL). ESLs can be created in the laboratory using 

small logs with EAB eggs either laid directly onto 

the log surface by females or, if eggs have been laid 

on filter paper, attached artificially to the log. ESLs 

can then be suspended from trees in the field. Eggs 

exposed in this manner, however, often suffer high 

levels of predation unless protected with screening or 

ribbon. 

Another method for assessing rates of egg 

parasitism in the field is carried out by scraping off 

outer sections of bark from ash trees and returning 

bark removed from delineated areas of the trunk to 

the laboratory (Bauer et al., 2012). There, samples 

are first placed in incubators for several weeks to 

allow live parasitoids time to emerge. Next, the bark 

scrapings are passed through standard window 

screening (~1 mm x 1 mm mesh) and the material 

passing through the screen is examined under a 

microscope to detect eggs and determine their fate 

(live, dead, dead parasitoid, emerged parasitoid, 

emerged EAB larvae, infertile egg). Eggs that have 

been parasitized often turn darker in color and 

contain droplets of meconium inside the egg shell, 

and parasitoids leave characteristic round exit 

holes. These two sources of information (emerged 

parasitoids and eggs found in screened material) are 

combined to estimate of parasitism. This procedure 

provides the best available estimate of parasitism, but 

it does not capture any estimate of predation rates 

on eggs. Predation (potentially by taxa such as ants 

or thrips) is indicated by large, jagged holes in the 
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145 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

eggs, and can potentially obscure previous parasitism 

(Duan et al. 2011b). Separate sampling methods are 

needed to estimate the extent of egg predation under 

field conditions. 

Larvae and pupae. Larvae and pupae are 

relatively easy to locate in comparison to the 

other EAB life stages. To begin with, when using 

experimentally established cohorts created from 

eggs laid on filter paper, hatching success can be 

ascertained by inspecting the paper for signs that the 

larvae chewed through it. If larvae do successfully 

emerge from eggs, four general sources of mortality 

can then be assigned to EAB larvae and pupae: 1) 

disease, 2) killed by tree resistance, 3) parasitism, 

and 4) predation (Fig. 2). Disease can be assigned 

by examining the cadaver for signs and symptoms 

of entomopathogenic fungi or other disease-causing 

pathogens (Liu and Bauer, 2006) (Fig. 2a). However, 

because diagnostic tests for pathogens are not done, 

however, this category also includes EAB killed by 

starvation or cannibalism. Tree resistance, which 

typically affects early (1st and 2nd) larval instars, can 

usually be identified by callous formation around the 

larval gallery (Fig. 2b). 

There are several approaches used to detect 

parasitism, which is most often identified in late (3rd 

and 4th) larval instars and pupae. These methods 

include examining galleries for meconium left by 

parasitoid larvae, or finding parasitoid larvae, pupae, 

adults, or parasitoid pupal exuviae in galleries (Fig. 

2c). In addition to detecting introduced parasitoids, 

the same approach also detects several native 

parasitoids that attack EAB in North America, and 

those parasitoids should also be considered in life 

table analyses, including Atanycolus spp., Balcha 

indica Mani and Kaul, Spathius floridanus Ashmead, 

and Phasgonophora sulcata Westw. (Bauer et al., 

2005; Duan et al., 2009; Duan et al., 2012c; Duan 

et al., 2013a). Even if there are no obvious signs of 

parasitism, any live larvae or pupae collected when 

debarking trees should be found and maintained in 

incubators for adult emergence and identification. 

Live larvae damaged during sampling should be 

immediately dissected to detect possible immature 

parasitoids. This may also be preferable even for the 

live undamaged larvae because many such larvae 

a b

c d

Figure 2. Examples of the four main mortality factors affecting 

EAB. Shown are: (a) disease/intraspecific competition; (b) 

killed by tree resistance; (c) parasitism, and (d) predation. 

(Photo credit: Jian Duan, USDA-ARS, and David Jennings, 

University of Maryland) 

die of fungal diseases during the prolonged rearing 

period required for them to complete their life cycle 

(Bauer et al., 2012). 

Predation from insectivorous birds such as 

woodpeckers generally occurs on late (3rd and 4th) 

larval instars and pupae (Cappaert et al., 2005c; 

Lindell et al., 2008; Jennings et al., 2013; Koenig et 

al., 2013). Woodpecker damage can be identified 

on the outside of the bark before peeling, and then 

galleries can be traced underneath to the point of 

attack (Fig. 2d). Because parasitism and predation 

both occur on late larval instars, there is a possibility 

that some evidence of parasitism could be lost 

through predation. Presently there does not appear 

to be any evidence that woodpeckers preferentially 

feed on parasitized or unparasitized larvae, but the 

number of parasitized larvae has been was found 

to be significantly higher when woodpeckers were 

excluded from trees with experimentally established 
CHAPTER 9: LIFE TABLE EVALUATION OF CHANGE IN EAB POPULATIONS DUE TO BIOLOGICAL CONTROL

146 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

Figure 3. Simulated additional parasitism rates required to reduce EAB R0 to <1 in Maryland 

(red lines) and Michigan (blue lines) (based on experimental cohorts at Legg and Harris 

Nature Center Parks in 2010). Solid lines represent larval parasitism, dashed lines represent 

egg parasitism. Black line represents R0

 =1, beneath which EAB population growth would 

be declining. 

cohorts of EAB (Jennings et al., 2013) , suggesting 

that parasitized larvae are taken. 

Adults. Estimating the mortality of EAB adults 

can be challenging. Natural sources of mortality 

likely include predation from insectivorous birds 

and disease, but these are difficult to quantify under 

field conditions. For the purposes of life table 

construction, the most effective way may be to use 

data collected from laboratory studies to parameterize 

the models. Such an approach was utilized by Duan et 

al. (2014), who assigned a mortality rate of 5% to EAB 

adults. 

eFFeCts oF BiologiCal Control 

on eaB popUlations 

In areas where EAB parasitoids have been released 

for several years there is evidence that some species 

(particularly T. planipennisi) are establishing and 

increasing in population size (Duan et al., 2013b). 

With few published studies examining the effects 

of these parasitoids on EAB population growth 

using a life table approach, it is difficult to make 

generalizations from the results. However, using 

the data available, we can manipulate life tables and 

investigate how EAB populations are projected to 

change under different scenarios. Specifically, we can 

use the data from published life tables to model what 

rates of egg and larval parasitism would be sufficient 

to reduce EAB population growth to non-pest levels. 

In Maryland, EAB first arrived in 2003 from 

EAB-infected ash nursery stock shipped from 

Michigan and sold in Maryland and Virginia. Despite 

an attempt to eradicate EAB in this region, EAB 

was considered established in Maryland in 2006 

and Virginia in 2008 (see Chapter 1). In Maryland, 

EAB populations from experimental cohorts were 

found to have R0

 values of 17.9 when woodpeckers 

were present and 19.2 when woodpeckers were 

excluded using caging (Jennings et al., 2013). Both 

of these growth rates are high, and they suggest that 

woodpecker predation does not contribute greatly 

to mortality at sites with a low to moderate EAB 

infestation. The main source of mortality at these 

newly colonized sites was tree resistance, and while 

parasitism was detected it was at relatively low levels. 

However, in New York (at study sites where EAB 

was established longer in comparison to those used 

in Maryland), where neither parasitism nor tree 

resistance were significant sources of mortality, R0 
CHAPTER 9: LIFE TABLE EVALUATION OF CHANGE IN EAB POPULATIONS DUE TO BIOLOGICAL CONTROL

147 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

values for wild populations were much higher (29.8 

and 50.5 when woodpeckers were able to feed on 

EAB stages and when woodpeckers were excluded, 

respectively) (Jennings et al., 2013). This suggests 

woodpecker predation can significantly reduce EAB 

population growth only at sites where EAB densities 

are high. 

In Michigan (at sites where EAB has been 

established for several years), life tables constructed 

by Duan et al. (2014) found that in the first 

generation of EAB studied R0

 values were similar to 

those in Maryland (16 for experimental cohorts and 

19.4 for wild populations). However, a large drop in 

R0

 was seen in the second generation (4.6 and 4.7 for 

experimental and wild cohorts, respectively), which 

coincided with an increase in the level of parasitism 

detected. Mortality was greater in later larval stages 

than in early ones, primarily because of parasitism 

from Atanycolus spp. and T. planipennisi. Host tree 

resistance and disease remained important for early 

larval stages, while woodpecker predation was the 

largest mortality factor for J-larvae. The results also 

suggest that experimental and wild cohorts of EAB 

may be used comparably for population studies 

if certain adjustments are made to account for 

potentially overlapping generations. 

Models using data from experimental cohorts at 

some of the sites in Maryland and Michigan suggest 

that if egg and larval parasitism can be increased 

then there is the potential to reduce EAB population 

growth to more manageable levels (Fig. 3). These 

models were constructed by increasing parasitism 

in increments of 10%, while re-adjusting the stagespecific mortality rate to keep it at the originally 

observed proportions. Results suggest that in 

Michigan, ~30% additional larval parasitism would 

be sufficient to cause a decline in EAB populations, 

while in Maryland it would take ~65%. An increase 

in egg parasitism of ~50% would be sufficient to 

reduce R0 <1 in both locations. While these models 

are simplistic, they serve to illustrate the utility of life 

table analyses. 

reFerenCes
 

Abell K. J., J. J. Duan, L. S. Bauer, J. P. Lelito, and R. G. 

Van Driesche. 2012. The effect of bark thickness 

on host partitioning between Tetrastichus 

planipennisi (Hymen: Eulophidae) and Atanycolus 

spp. (Hymen: Braconidae), two parasitoids 

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Chapter 10: risK to ash From emerald ash Borer: 


Can BiologiCal Control prevent the loss oF ash stands?
 

Jian J. Duan1, Roy G. Van Driesche2, Leah S. Bauer3, Daniel M. Kashian4, and Daniel A. Herms5 

1

USDA, Agricultural Research Service, Beneficial Insects Introduction and Research Unit, Newark, Delaware 19731
 

2

Department of Environmental Conservation, University of Massachusetts, Amherst, Massachusetts 01003
 

3

USDA, Forest Service, Northern Research Station, East Lansing, Michigan 48823
 

4

Department of Biological Sciences, Wayne State University, Detroit, Michigan 48202
 

5

Department of Entomology, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster, Ohio 44691
 

introdUCtion 

Ash trees (Fraxinus spp.) are an important 

components of both natural forests and urban 

plantings in the United States and Canada (Federal 

Register, 2003; Nowak et al., 2003). There are 

approximately16 species of Fraxinus native to North 

America (Harlow et al., 1996; USGS, 2014), each 

adapted to different ecological niches across a range 

of climates zones, soil types, and moisture gradients 

(Eyre, 1980). This abundant and diverse ash resource 

provides economic benefits, with ash timber alone 

valued at $282 billion (Nowak et al., 2003). For 

instance, green ash (F. pennsylvanica Marsh.), the 

most widely distributed ash in North America, is 

a fast growing, moderately shade tolerant tree that 

grows in mixed hardwood stands along river bottoms 

and wetlands, in small lowland groves, or in upland 

mesic sites. It was planted extensively throughout 

North America as an ornamental landscape and 

street tree due to its rapid growth and hardiness, 

and as agricultural shelterbelts for livestock shelter 

and soil conservation (MacFarlane and Meyer, 

2005; D’Orangeville et al., 2008). Ash trees are also 

a valuable ecological component of the deciduous 

forests of eastern North America, and provide 

food, cover, nesting sites, and habitat for mammals, 

birds, insects, and other organisms (Poland and 

McCullough, 2006; Gandhi and Herms, 2010; Koenig 

et al., 2013). 

Clearly, the ecological and economic value of ash 

in North America justifies appropriate measures for 

its protection against the invasive emerald ash 

borer (EAB, Agrilus planipennis Fairmaire), which 

threatens the persistence of ash in mixed hardwood 

stands. In this chapter, we will first review various 

ecological factors that may affect the potential for 

ash mortality due to EAB. We will then examine the 

population dynamics of EAB in its newly invaded 

region (North America) vs. its native range (northeast 

Asia), and attempt to identify critical or key biotic 

factors that may be employed or manipulated to 

suppress EAB population growth. Finally, we will 

review the current EAB biological control program 

that involves introduction and establishment of 

hymenopteran parasitoids from northeast Asia. In 

particular, we will examine whether natural enemies 

(parasitoids) can maintain EAB populations at an 

equilibrium density low enough to allow ash to 

regenerate and recover. 

FaCtors aFFeCting ash risK 


From eaB invasion
 

Ash trees were once relatively free of serious, major 

diseases (except for ash yellows in some limited areas) 

and insect pests in North America until the arrival of 

EAB (Barnes and Wagner, 2003; Pugh et al., 2011). 

EAB was first detected in North America in Michigan 

in 2002, and as of February 2014, it had been detected 

in 22 U.S. states and two Canadian provinces, killing 

millions of ash trees (see reviews in Herms and 

McCullough, 2014; ) (Fig. 1) (see reviews in Herms 

and McCullough, 2014). All ash species native to 

North America that have been encountered by EAB 

to date are susceptible to EAB, including the most 
CHAPTER 10: RISK TO ASH FROM EAB: CAN BIOLOGICAL CONTROL PREVENT THE LOSS OF ASH STANDS?

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

common species: green, white (F. americana L.), and 

black (F. nigra Marsh.) as well as the less common 

blue (F. quadrangulata Michx.)and pumpkin ash (F. 

profunda [Bush] Bush). Although there is increasing 

evidence that EAB will attack all species of Fraxinus, 

innate susceptibility of ash trees varies with a variety 

of ecological factors such as physiological condition, 

habitat type, and species. Below are some ecological 

factors that may affect the likelihood of ash risk from 

EAB invasions in North America. 

Figure 1. Mortality of overstory green ash trees caused by 

emerald ash borer in 2003, Kensington Metro Park, Brighton, 

Michigan. (Photo credit: Leah Bauer) 

Ecological Habitats: Natural Forest vs.Urban 

Plantings 

After its accidental introduction into North America, 

EAB established on ash trees in urban areas and 

subsequently spread into nearby natural forests 

(Haack et al., 2002; Michigan State University, 

2014; Canadian Food Inspection Agency, 2014). 

Although EAB is a strong flier, long-range dispersal 

occurs primarily through human activities, often 

along roadways lined with ash trees. EAB spread 

has appeared to follow a wave pattern across the 

landscape through short-distance natural dispersal 

and as well as long-range dispersal assisted by human 

activities (Taylor et al., 2010; Prasad et al., 2010; 

Kashian and Witter, 2011). In Russia (Duan et al., 

2012a; Straw et al., 2013) and northeastern China (Liu 

et al., 2007; Wei et al., 2004, 2007; Wang et al., 2010), 

EAB outbreaks have been noted primarily on North 

American ash trees planted in plantations or as street 

trees. EAB populations have the potential to disperse 

quickly in urban areas due to widespread planting 

of susceptible ash species and human-assisted 

movement and storage of EAB-infested materials (see 

review in Herms and McCullough, 2014). 

Age of Ash: Mature Trees vs Saplings 

Although the diameter at breast height (DBH) of ash 

trees does not significantly influence the probability 

of EAB oviposition or infestation (Marshall et al., 

2011; Klooster et al., 2014; Jennings et al., 2014), EAB 

infestations in North America have first killed mature 

(canopy) ash trees rather than smaller understory 

saplings (Cappeart et al., 2005). Recent studies have 

further shown that ash saplings with DBH <2.5 cm 

are rarely attacked by EAB (Marshall et al., 2011, 

2013). It is conceivable that young ash saplings 

have both physical (e.g., smooth-bark surface) and 

chemical (secondary compound) characteristics that 

are less attractive to EAB oviposition than canopy ash 

trees (e.g., Marshall et al., 2013). It is also possible 

that saplings with stem diameters smaller than <2.5 

cm are too small to be colonized and killed. Klooster 

et al. (2014) found that mortality of green, white, and 

black ash trees in mixed stands with stems equal to 

or greater than 2.5 cm exceeded 99% in southeastern 

Michigan forests by 2009, suggesting that there is little 

resistance or tolerance in these ash populations, and 

that EAB does not discriminate based on chemical or 

physical attributes when populations are high. 

Species and Variety 

Liu et al. (2003), studying EAB in China, reported 

higher EAB densities in North American species 

(green ash and velvet ash, F. velutina Torr.) than 

in Asian species (F. chinensis Roxb.; F. chinensis 

var. rhynchophylla). In a common garden trial 

in Michigan, Rebek et al. (2008) confirmed the 

presence of interspecific variation in responses to 

EAB infestations between the Asian (F. mandschurica 

Rupr.) and North American species (F. pennsylvanica 

and F. americana). Exposed to similar EAB 

infestation pressure, the Asian species, Manchurian 

ash, suffered far less mortality and yielded far fewer 
CHAPTER 10: RISK TO ASH FROM EAB: CAN BIOLOGICAL CONTROL PREVENT THE LOSS OF ASH STANDS?

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Figure 2. Inter-species variation in ash resistance to emerald 

ash borer infestation in its native range (Vladivostok, Russia). 

North American green ash trees (F. pennsylvanica) planted in 

the 1970s on the left side of the tramline show late stages of 

EAB infestation symptoms (canopy declines, exit holes, bark 

splits etc.). Oriental ash (F. rhynchophylla or F. manschurica) 

were planted in the 1980s on the opposite side of the tramline 

show little signs of EAB infestation. (Photo credit: Jian Duan) 

adult beetles than several cultivars of North American 

green and white ash. Duan et al. (2012a) also 

observed similar interspecific variation in resistance 

to EAB infestations between the Asian species 

Fraxinus rhynchophylla Hance and North American 

green ash (F. pennsylvanica) in the Russian Far East, 

the possible native range of EAB (Fig. 2). The higher 

resistance of Asian ash may have resulted from a long 

co-evolutionary history with EAB (Liu et al., 2003; 

Rebek et al., 2008), thereby restraining EAB densities 

within its native range. 

Seed Banks and Regeneration 

Kashian and Witter (2011) examined the potential 

for ash canopy tree recovery in EAB-affected stands 

from 2007 to 2009, measuring regeneration at 45 

sites in southeastern Michigan (USA) following stand 

decline from EAB infestation. White, green, or black 

ash regeneration was abundant at all sites, particularly 

of the smallest ash height classes, but new seedling 

density dropped significantly between 2007 and 

2009. This dramatic decrease in new seedlings was 

interpreted to be the result of a depleted seed bank, 

because few or no nearby mature ash trees existed to 

provide seed. Recent sampling in small pure stands 

of green ash suggest that seed production during ash 

mast years (on both surviving mature ash and sprouts 

from killed trees) may be sufficient to maintain a 

significant – though greatly reduced – pool of ash 

regeneration that may allow ash to persist at low 

levels (D. M. Kashian, unpub.). It remains to be seen 

if ash regeneration will be high enough to repopulate 

sites with mature trees in Michigan where pre-EAB 

ash density was lower, especially because the future 

dynamics of EAB populations in the region are still 

uncertain. 

In another study, Klooster et al. (2014) conducted 

extensive soil sampling in southeastern Michigan 

forests located within 45 km of the epicenter of the 

infestation and found no seeds after 2007, suggesting 

depletion of the seed bank. Once mortality of ash 

with stem diameters greater than 2.5 cm exceeded 

99% in 2009, they observed no newly germinated 

seedlings (with cotyledons) either inside or outside 

their plots, which is also consistent with a depleted 

seed bank. They did observe that ash mortality 

decreased slightly in 2010 to about 97% as smaller 

saplings grew large enough to reach the 2.5 cm size 

class. However, EAB trapping revealed that a lowdensity EAB population continued to persist on this 

cohort of saplings. Based on these patterns, Klooster 

et al. (2014) concluded that the long-term fate of 

ash in these sites will depend on the establishment 

of a dynamic equilibrium between current ash 

regeneration, EAB, and its natural enemies. 

Natural Enemies 

Several species of larval and egg parasitoids have 

been discovered in the native range of EAB. Field 

studies in Asia show that these natural enemies 

cause up to ~70% parasitism of EAB larvae or eggs 

in EAB’s native range (Liu et al., 2003, 2007; Duan 

et al., 2012a). It is very likely that these Asiatic 

natural enemies exert important top-down effects 

on EAB population dynamics and may potentially 

limit outbreaks of EAB in Asia to levels that do not 
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cause significant mortality to ash. However, natural 

enemies do not appear to have prevented EAB 

outbreaks on highly susceptible North American ash 

species that were planted in China (Liu, 1966; Wei et 

al., 2004). In contrast, parasitism by North American 

parasitoid species was minimal (<5%) when EAB was 

first detected in Michigan and is often low in other 

newly infested areas (e.g., Bauer et al., 2005; Duan et 

al., 2009, 2012b, 2013a). This lack of effective natural 

enemies in North America was the justification for 

introduction of Asian parasitoids into the United 

States for classical biocontrol of EAB. Whether or not 

the newly introduced EAB parasitoids will provide 

sufficient reduction of EAB populations to allow 

recovery or regeneration of ash needs continued 

study as part of the EAB biological control program. 

eaB popUlation dynamiCs in 

neWly invaded and native ranges 

The invasion wave of EAB in ash-dominated forests 

of a newly invaded region has been described as 

having three main stages: the cusp, crest, and core 

(Burr, 2012; Burr and McCullough, 2012). The cusp 

phase occurs at newly infested sites in the first few 

years as EAB populations slowly build, before their 

numbers rapidly increase and cause tree mortality in 

the crest phase. The core phase then occurs around 

10 years after the initial infestation, by which time 

most ash trees have died and EAB populations have 

crashed. Burr (2012) characterized EAB population 

density and conditions of green ash overstory and 

regeneration from 2010 to 2011 in 24 forests sites in 

Michigan, which were at the three different stages 

of the EAB invasion wave. Recent studies suggest 

that host tree mortality (or depletion of host tree 

resources) is the major factor driving the invasive 

population of EAB to emigrate or disperse into new 

areas or forests (Mercader et al., 2009; Burr, 2012; 

Burr and McCullough, 2012). However, longterm studies of EAB population dynamics and its 

underlying regulation factors at different invasion 

stages are currently lacking in North America. 

Evidence gathered thus far in the native range of EAB 

has shown that EAB outbreaks in northeastern Asia 

are rare events in natural forests, and outbreaks occur 

primarily in isolated plantations or urban plantings 

of mostly North American ash (F. pennsylvanica, F. 

americana or F. velutina) (Wei et al., 2004). While 

infestations within the native range of EAB can 

occasionally cause significant ash mortality in urban 

plantings or plantations, no important outbreaks 

(comparable to those in North American forests) have 

been recorded in canopy ash in native Asian forests 

(Liu et al., 2007; Williams et al., 2010; Duan et al., 

2012a). Recent ecological studies of EAB population 

dynamics in in the Russian Far East and northeastern 

China suggest that natural enemies (larval and egg 

parasitoids) and host tree resistance are the two key 

factors that regulate EAB population dynamics in 

its native range (Liu et al., 2003, 2007; Duan et al. 

2012a), and thus the lack of these two key mortality 

factors in North America may explain the severity 

of EAB damage there. Understanding the ecological 

mechanisms or key factors that regulate EAB 

population dynamics in both its native range and 

newly invaded areas will be critical for developing 

sustainable strategies for managing this invasive pest 

in North America. 

Can BiologiCal Control 

signiFiCantly deCrease 

ash mortality? 

The Current Status 

Classical biological control was initiated shortly after 

EAB detection in the United States due to the failure 

of eradication efforts (see Chapter 4). This program 

has introduced and achieved establishment of three 

exotic parasitoids (two larval parasitoids and one egg 

parasitoid) sourced from part of the native range in 

northeastern China (see Chapter 5). Field surveys in 

Michigan, Maryland, and New York show that one of 

the released larval parasitoids, Tetrastichus planipennisi Yang, became widely established on EAB populations at both release and nearby control sites 3-4 years 

after release (Bauer et al., 2008, 2009, 2010; Gould et 

al., 2011; Duan et al., 2012b, 2013b; Jennings et al., 

2013). Duan et al. (2013b) showed that parasitism 

of EAB larvae by T. planipennisi in central Michigan 

steadily increased from <1% in the first year (2008) 
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BIOLOGY AND CONTROL OF EMERALD ASH BORER

 

after field releases to ~21% (release plots) and 12% 

(control plots) four years later (by 2012). While the 

introduced egg parasitoid, Oobius agrili Zhang and 

Huang, appears to have also established primarily 

at release sites in central Michigan and Maryland 

following releases between 2008 – 2011, rates of EAB 

egg parasitism varied from <5% to as high as ~28% 

among different release sites and years after field 

releases (Duan et al., 2010, 2012b; L.S. Bauer, unpublished data) and appear to be increasing. In contrast, establishment of the braconid larval parasitoid 

Spathius agrili Yang is less certain, and observed levels 

of field parasitism by this species have been minimal 

(<0.1%). 

Currently, levels of parasitism by these introduced 

parasitoids are still much lower than those observed 

in their native range (Liu et al., 2007; Duan et al., 

2012a; Yang et al., 2010). This is most likely due to 

the limited number of the wasps released in the initial 

phases of the program (2008-2011) and the short 

period of time available for the released parasitoids’ 

populations to increase. With release of larger 

numbers of these parasitoids in North America in 

the next few years, it is possible that these parasitoids 

will greatly increase in abundance and inflict levels 

of EAB larval and egg parasitism that are comparable 

to those observed in their native ranges. With the 

development of effective mass-rearing methods, it is 

also conceivable that these biological control agents, 

particularly the egg parasitoid O. agrili, could be 

released in large numbers as a means of effectively 

preventing EAB populations from reaching levels able 

to kill ash trees, at least on a local scale. 

The Premise of EAB Biological Control 

The premise of EAB biological control is that EAB 

outbreaks are rare in China and other parts of EAB’s 

native range, in part because of the presence there 

of more effective natural enemies that suppress 

outbreaks before they occur. It is commonly noted 

that there are many isolated stands of healthy saplings 

of North American ash species (green and velvet, 

respectively) in urban areas of the Russian Far East 

and China. It is thus plausible that EAB parasitoids 

in this region might have protected these susceptible 

ash trees at two different phases. First, saplings of 

susceptible ash species in Asia might be colonized 

initially at low levels of EAB because there are fewer 

beetles coming from resistant trees, which would not 

be the case in North America. Moreover, survivorship 

of F1 immature EAB stages on these saplings might be 

reduced by a rapid increase of parasitoid populations 

due to shorter handling times for parasitoids to attack 

hosts on saplings. This could retard EAB buildup on 

susceptible ash trees in Asia. Second, the abundance 

of EAB parasitoids in the native range may in fact 

allow their populations to increase rapidly via 

numerical response to incipient infestations of EAB 

on susceptible ash species and thus directly protect 

the trees while beetles are at relatively low density. 

Factors Affecting the Efficacy of EAB Biological 

Control 

The question then arises whether these introduced 

parasitoids can successfully establish in North 

America and effectively reduce the invasive EAB 

population to a sufficiently low level to allow ash for 

regeneration and recovery of ash overstory trees in 

forests. See Figure 3, a hypothetical model of EAB 

population dynamics with successful EAB biological 

control. 

The following ecological factors are most likely 

to influence the success of the current EAB biological 

control program in North America: 

Climatic matching and adaptability of the 

introduced parasitoids in North America. 

The adaptability of the introduced Asiatic parasitoids 

to the climatic and other ecological conditions (e.g., 

host’s phenology) in North America would have 

profound impacts on their successful establishment 

and efficacy in controlling EAB populations. Climatic 

matching analysis showed that the climatic conditions 

in northeast China, where T. planipennisi and O. agrili 

originated, generally matches that of the midwestern 

and northeastern United States, where EAB has firmly 

established (Federal Register, 2007). Thus, it is not 

surprising that both species appear to have become 

well established in Michigan and other midwestern 

states shortly after their field releases. However, the 

establishment of the other Chinese larval parasitoid, 

S agrili, has been less certain in Michigan and other 

northern states in the United States. This is most 
CHAPTER 10: RISK TO ASH FROM EAB: CAN BIOLOGICAL CONTROL PREVENT THE LOSS OF ASH STANDS?

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

Figure 3. A schematic illustration of emerald ash borer population dynamics 

with successful biological control: Released parasitoids should reduce the EAB 

population to a low “equilibrium” density that allows ash regeneration and 

recovery to canopy trees. 

Figure 4. Comparison of net reproductive rate (R0) of an emerald ash borer 

population in North America vs. Asia when different levels of dominant mortality 

factors are present or absent from life tables constructed in two study periods 

(2008–2009 and 2009–2010) in central Michigan, the epicenter of the North 

American invasion. R0

 > 1 results in population increase; R0 = 1 results in a stable 

population; R0

< 1 results in successful suppression of EAB population growth. 
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likely because the source of S. agrili was further south 

in Tianjin, China (southeast of Beijing on the coast) 

where temperatures are moderated by the China 

Sea. In contrast to S. agrili, the congener Spathius 

galinae Belokobylskij & Strazanac was collected 

from the Russian Far East and is thus likely to be 

more cold tolerant than S. agrili (Duan et al., 2012a; 

Belokobylskij et al., 2012; Khun et al., 2013). Climate 

matching analysis indicates that the climate in the 

central region of the United States is potentially more 

suitable for S. agrili than the more northern areas 

where most releases have been made to date. Climate 

matching analysis further indicates that the portion of 

the US suitable for S. galinae is considerably further 

north than for S. agrili (Gould and Duan, 2013). 

The size or age of ash trees to be protected. 

Ash trees are fast growing, an expected lifespan of 200 

to 300 years, and normally produce seeds after 30 – 40 

years (Garden Guide, 2014). Although the size or age 

of ash trees (often measured as DBH) does not appear 

to significantly influence the probability of EAB 

infestation or tree mortality (see previous section), 

bark thickness as a function of tree age or size can 

have significant effects on the efficacy of EAB larval 

parasitoids in finding and attacking host larvae. For 

example, Abell et al. (2012) showed that EAB larvae 

infesting ash trunks with a DBH>11.2 cm are rarely 

parasitized by the larval parasitoid T. planipennisi 

because this species has an ovipositor ranging in 

length from 2.0-2.5 mm and thus cannot oviposit 

through bark that is thicker than 3.2 mm. Based 

on these findings, Abell et al. (2012) recommend 

releasing T. planipennisi only in early-successional 

stands with small ash trees, but not in mature forests 

where ash was mostly larger. For protection of 

large ash trees (DBH >12 cm), parasitoids such as 

S. galinae, with much longer ovipositors (4.5 – 5.5 

mm) should be considered for use in EAB biocontrol 

programs. Based on regression analysis of bark 

thickness and DBH (Abell et al., 2012), it is estimated 

that S. galinae could successfully oviposit through 

bark in trees up to 29 mm DBH, greatly enhancing its 

usefulness as a biological control agent. 

Level of ash tree resistance to EAB. 

Host tree resistance is a dominant factor that can have 

a “bottom-up” effect on EAB population growth in 

its native range (see previous section). Levels of host 

tree resistance will also have effects on the success 

of natural enemies, particularly larval parasitoids, 

in controlling EAB populations that have already 

infested ash trees. For example, there is strong 

evidence that EAB larvae develop more slowly and 

more often express semi-voltinism in healthy ash 

trees compared to artificially girdled, or previouslyinfested ash trees (McCullough et al., 2009; Duan 

et al., 2010). The slower larval development and a 

semi-voltine life cycle may provide a much wider 

of window for foraging parasitoids to attack host 

larvae, and thus result in higher control efficacy. A 

population dynamics model parameterized with 

observed larval and egg parasitism rates (~60%) in 

Asia, showed that natural enemies in Asia can quickly 

reduce the rate of EAB population growth when 

accompanied by moderate to high levelsof host plant 

resistance (Fig. 4) (JJD unpub; see also Chapter 9). 

ConClUsions 

Ash trees were once relatively free of serious, major 

diseases and insect pests in North America until the 

arrival of EAB, which was first detected in North 

America in Michigan in 2002. As of February 2014, 

EAB had been detected in 22 U.S. states and two 

Canadian provinces, killing millions of ash trees. 

The ecological and economic value of ash justify 

appropriate measures to manage this invasive pest, 

and the current EAB biological control program was 

initiated shortly after its detection in the United States 

due to the failure of eradication efforts. The premise 

underlying the classical EAB biological control 

program is that EAB outbreaks are rare in China 

and other parts of its native range, in part because 

effective natural enemies prevent or quickly suppress 

EAB outbreaks. 

The EAB biological control program has resulted 

in the introduction and successful establishment 

in North America of three exotic parasitoids (two 

larval parasitoids, T. planipennisi and S. agrili, and 

one egg parasitoid, O. agrili) sourced from the native 

range of EAB in northeastern China. An additional 

species of EAB parasitoid, S. galinae, is also currently 

under review for potential release against EAB in the 
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northeast United States. The key question is whether 

these introduced parasitoids, once established, can 

effectively regulate the EAB population at sufficiently 

low densities such that an equilibrium can be 

maintained between EAB and its natural enemies that 

permits survival and regeneration of ash in North 

American forests. 

To answer this question, we examined various 

factors that may potentially affect the risk to ash 

from EAB invasion, including population dynamics 

of EAB in both the newly invaded region and its 

native range (northeast Asia), and dominant biotic 

factors that regulate EAB populations in its native 

range. We suggest that ash tree resistance and 

natural enemies (parasitoids) are the two dominant 

biotic factors that have the potential to regulate EAB 

population dynamics. A population dynamics model 

parameterized with the egg and larval parasitism rates 

(~ 60%) observed in EAB’s native range suggests that 

natural enemies coupled with moderate to high levels 

of host plant resistance has the potential to reduce the 

growth rate of EAB populations below replacement, 

and thus maintain EAB populations at low-density, 

equilibrium levels, which should permit survival and 

regeneration of ash in the aftermath of EAB invasion 

in North America forests. 

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

Chapter 11: FUtUre direCtions in eaB-aFFeCted Forests 

Deborah G. McCullough1, Roy Van Driesche2 and Therese M. Poland3 

1

Department of Entomology & Dept. of Forestry, Michigan State University, Lansing, Michigan 48824; mccullo6@mail.msu.edu
 

2

Department of Environmental Conservation, University of Massachusetts
 

3

Northern Research Station, USDA Forest Service
 

The ability of natural enemies to slow emerald 

ash borer (EAB), Agrilus planipennis Fairmaire 

(Coleoptera: Buprestidae), population growth in 

a given area will play a major role in determining 

whether many native ash species can persist as 

functional components of forest ecosystems. 

Population growth of EAB, like that of any 

other organism, is determined by reproduction, 

development rate, and survival at each stage of 

development. Fecundity of female EAB is relatively 

high when compared to other phloem-feeding 

Agrilus species. For example, A. difficilis Gory can 

produce 36 eggs per female (Akers et al., 1986), A. 

anxius Gory, 55 eggs (Rutledge and Keena, 2012), A. 

auriventris Saunders, 140 eggs (Huangfu et al., 2007), 

while a female A. auroguttatus Schaeffer may produce 

575 eggs (Lopez and Hoddle, 2014). In laboratory 

settings, EAB females can lay more than 275 eggs over 

the course of their life span. Although egg viability 

tends to diminish over time, even in the wild, on 

average, EAB can probably produce at least 40-60 

offspring per female. 

Most EAB larvae develop in a single year, but in 

newly infested ash that are relatively healthy a high 

proportion of larvae require two years to develop 

(Siegert et al., 2010; Tluczek et al., 2011), initially 

slowing the new population’s growth rate (Mercader 

et al., 2011). Populations of EAB in northern latitudes 

where summers are short may also be more likely 

to require two years for development, a pattern 

previously observed with A. anxius (Barter, 1957). 

In stressed ash, including trees injured by increasing 

densities of EAB larvae, however, all or nearly all EAB 

develop in a single year (Tluczek et al,. 2011). 

Like other phloem-feeding insects, the survival of 

larvae of EAB is primarily limited by the availability 

of phloem of its host tree. Using data from several 

field studies, Mercader et al. (2011) estimated that 

an EAB larva requires approximately 10 cm2

 of 

ash phloem to complete development. Similarly, 

McCullough and Siegert (2007) reported an average 

of approximately 89-105 adult EAB could develop 

per m2

 of phloem in white ash (Fraxinus americana 

L.) or green ash (Fraxinus pennsylvanica Marshall). 

Canopy decline generally becomes apparent at a 

density of 25-35 EAB per m2

 (Anulewicz et al., 2007). 

Ash phloem available for larval feeding increases 

rapidly with the diameter at breast height (dbh) of the 

tree. For example, using methods of McCullough and 

Siegert (2007), a tree with a dbh of 30 cm can produce 

approximately 1335 adult EAB, while a 60 cm tree 

can produce 6285 beetles. Of course, not every m2

 of 

phloem will produce 90-100 adult EAB beetles. At 

the peak of the invasion, individual trees can harbor 

200-300 early stage larvae per m2

 (Tluczek et al., 

2011, Tanis and McCullough 2015), but intraspecific 

competition for phloem results in high mortality, 

typically of third instars. Nevertheless, when ash, 

particularly large ash, are abundant, EAB density in 

a given area will be very high during the peak of the 

invasion wave. 

Given that few options are available for reducing 

female fecundity or slowing development of EAB, 

effective control tactics must limit survival of eggs, 

larvae, or adult beetles. Systemic insecticides protect 

landscape ash trees by substantially reducing survival 

of EAB adults and larvae, but these products are 

obviously not likely to be used in forests. Mortality 

of EAB attributable to parasitism and predation 

varies considerably among sites and among trees 

within sites. Relatively high rates of egg parasitism 

(ca 20%) (Abell et al., 2014), larval parasitism (10­

70%) (Cappaert and McCullough, 2009; Duan et al., 

2013; Tanis and McCullough, in press 2015), and 
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166 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

woodpecker predation (22-85%) (Lindell et al., 2008; 

Jennings et al., 2013; Duan et al., 2013; Flower at 

al., 2014; Tanis and McCullough, 2015) have been 

recorded at some sites in Michigan and Ohio. Duan 

et al. (2014) reported that in some Michigan sites, 

population growth rates for experimental (artificially 

established) EAB cohorts dropped from an R0 

value of 16.0 to 4.7 and from 19.4 to 4.6 for wild 

EAB cohorts. This drop, however, also reflects the 

progression of ash mortality at these sites. Mortality 

rates for overstory green ash, white ash and black ash 

(Fraxinus nigra Marshall) trees in much of southeast 

Michigan exceed 90% and few trees >10 cm dbh 

remain alive (Burr and McCullough, 2014; Flower et 

al., 2013; Knight et al., 2013; Klooster et al., 2014). 

Decreased EAB population growth rates, therefore, 

reflect the diminished availability of ash phloem for 

larval development together with increased mortality 

from natural enemies (Duan et al., 2014). 

The cumulative influence of mortality due to 

native and introduced natural enemies on EAB 

population trajectories is not yet clear, particularly 

in areas where the EAB invasion is relatively recent. 

Populations of EAB in southeast Michigan were 

established for more than a decade before the first 

introductions of Asian parasitoids (Gould, 2007) and 

the first observations of significant larval parasitism 

by native Atanycolus spp. (Liu et al., 2003; Cappaert 

and McCullough, 2009; Siegert et al., 2014). In 

states with more recent infestations, however, Asian 

parasitoids have been introduced within a few years 

of detection. Whether earlier introduction and 

establishment of Asian parasitoids will effectively 

slow the progression of ash mortality in these areas 

remains to be seen. 

Many of the Michigan stands decimated by EAB 

are characterized by abundant ash regeneration, 

including seedlings and saplings. Although ash 

saplings down to 2.5 cm in diameter can be colonized 

by EAB (Cappaert et al., 2005), trees <10 cm in 

diameter often escape colonization even during the 

peak of the EAB invasion wave (Herms et al., 2010; 

Burr and McCullough, 2014; Klooster et al., 2014; 

Smith et al., in press 2015). The fate of these young 

trees will likely determine whether ash persists as a 

functionally viable component of forest ecosystems in 

North America. Ash trees must be at least 8-10 cm in 

diameter before they begin to produce seed (Kennedy, 

1990), and frequency of seeding years varies among 

ash species. Seed crops can be heavy, but losses from 

unfilled seeds and seed predation (e.g., ash seed 

weevils [Lignyodes spp.]) can be substantial (Solomon 

et al., 1993), and seeds do not persist in the seed bank 

over time (Klooster et al., 2014). Ash seedlings are 

tolerant of shade and may persist in closed canopy 

stands for several years (Kennedy, 1990). As ash 

mature, they become increasingly intolerant of shade, 

and generally require full or nearly full exposure 

to sun to reach the overstory (Baker, 1949; Gucker, 

2005). Canopy gaps resulting from mortality of 

overstory ash can facilitate recruitment of young ash 

if gaps are not filled by lateral in-growth of other 

overstory trees (Bartlett and Remphrey, 1998, Burr 

and McCullough 2014) or regeneration of competing 

species (Flower et al., 2013, Smith et al., 2015). 

The ability of natural enemies, including native 

and introduced parasitoids, to prevent young ash 

from being killed by EAB may play a critical role in 

the long term survival and persistence of ash across 

much of North America. Density of EAB in a local 

area clearly declines as ash trees, particularly large ash 

trees, are killed. Effects of egg and larval parasitoids 

on EAB survival may become more pronounced in 

these areas after the EAB invasion wave goes through 

and the availability of ash phloem to support EAB has 

dropped substantially. Complete mortality of EAB life 

stages is not likely to be necessary; in general, most 

ash trees are remarkably resilient and tolerate a low 

level of larval feeding (McCullough et al., 2015). Thus, 

while ash may no longer function as a dominant 

overstory species, natural enemies may enable ash 

trees to persist at some level, providing food and 

habitat for populations of native insects and mites 

that are ash specialists (see Chapter 2). The consistent 

preference for small diameter trees demonstrated 

by Tetrastichus planipennisi Yang (Hymenoptera: 

Eulophidae), one of the introduced larval parasitoids 

(Abell et al., 2012; Duan et al., 2013), may be 

particularly beneficial in this regard. 

Given the current and potential impacts of EAB 

in North America, biological control research and 

evaluation efforts must continue. Possible effects 
CHAPTER 11: FUTURE DIRECTIONS IN EAB-AFFECTED FORESTS

167 

BIOLOGY AND CONTROL OF EMERALD ASH BORER

of interspecific differences among North American 

ash in resistance to EAB and the implications of 

these differences for biological control warrant 

consideration. Blue ash, Fraxinus quadrangulata 

Michx., growing on fertile sites, for example, 

appears to be relatively resistant to EAB, while 

black ash is highly vulnerable to EAB (Tanis and 

McCullough, 2012; Klooster et al., 2014; Herms and 

McCullough, 2014). Biological control agents may 

be more successful at a blue ash site because of its 

inherent higher resistance to EAB. Conversely, at 

sites dominated by black ash, introduced parasitoids 

may be overwhelmed and unable to demonstrate 

any numerical response to EAB before all or nearly 

all trees are killed. Evaluating factors associated 

with relative resistance and vulnerability of different 

ash species could have important implications for 

identifying sites where introduced parasitoids are 

likely to be most effective. 

In urban, residential, and even rural areas, effects 

of combining two or more EAB management tactics 

should be studied. Systemic insecticides, including 

products with emamectin benzoate, azadiractin, 

dinotefuran, or imidacloprid, are translocated in 

xylem to the canopy branches and foliage (MotaSanchez et al., 2009; Tanis et al., 2012). In contrast to 

cover sprays of insecticides applied to the outer bark, 

when systemic materials are used, egg parasitoids, 

such as the introduced Oobius agrili Zhang and 

Huang (Hymenoptera: Encyrtidae), will not 

encounter the insecticide. Larval parasitoids, whether 

native or introduced, will not attack dead EAB larvae 

nor will woodpeckers attempt to prey on dead larvae. 

Using systemic insecticides may therefore offer two 

benefits: ash trees treated with an effective product 

are protected from EAB injury and insecticidereductions in overall EAB density may cause 

parasitoids or predators to concentrate their efforts 

on infested but untreated trees. The combination 

of systemic insecticides and natural enemies could 

yield an additive effect or perhaps even a synergistic 

effect if natural enemy reproduction or host searching 

behavior is enhanced (Barclay and Li, 1991; Suckling 

et al., 2012). Understanding more about how to 

optimize the spatial distribution of trees treated with 

systemic insecticides in a given locality to enhance 

parasitism or predation rates could be productive. 

For example, field studies consistently show girdled 

ash trees are highly attractive to adult EAB, especially 

in recently infested sites (McCullough et al., 2009a,b; 

Mercader et al., 2013). Opportunities may exist to 

employ girdled or stressed ash to concentrate both 

EAB and parasitoid populations in selected areas. 

Much remains to be learned about native 

parasitoids, including their host-seeking behavior, 

cues that elicit parasitism, and the ability of these 

species to learn and adapt to a new host. Most native 

parasitoids and insect predators of phloem-feeding 

beetles are opportunistic habitat specialists, rather 

than host specialists (Kennedy and McCullough, 

2002) and, as such, may be capable of developing on 

many species, genera, and even families of insects 

(but see Taylor et al., 2012). Native parasitoids 

including Atanycolus spp., Phasgonophora sulcata 

Westwood (Hymen.: Chalcididae), and Spathius 

floridanus Ashmead (Hymen.: Braconidae), while 

not well studied, are frequently recovered from trees 

colonized by native wood- or phloem-borers and in 

some areas, parasitism of EAB larvae by one or more 

native species is increasing (Duan et al., 2012). 

Many parasitoids are adept at learning 

combinations of olfactory and visual cues associated 

with potential host insects and modifying their 

responses accordingly (Turlings et al., 1993). As an 

invasive insect population spreads, opportunities for 

native parasitoids to encounter and adapt to the new 

invader increase (Vet and Groenewold 1990; Turlings 

et al., 1993; Grabenweger et al., 2010). Assemblages 

of native parasitoids may respond and adapt to an 

invader relatively quickly, but their ability to affect 

dynamics of an invasive species varies considerably. 

For example, native generalist parasitoids quickly 

adapted to light brown apple moth, Epiphyas 

postvittana (Walker) (Lepidoptera: Tortricidae) in 

California and high parasitism rates contributed 

to population suppression (Wang et al., 2012). In 

contrast, native parasitoids had little effect on citrus 

leafminer (Phyllocnistis citrella Stainton [Lepidoptera: 

Gracillariidae]) populations in Spain and responded 

in a negative density-dependent manner to high pest 

populations (Vercher et al., 2005). Research on the 

ability of native parasitoids to adapt and respond to 
CHAPTER 11: FUTURE DIRECTIONS IN EAB-AFFECTED FORESTS

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BIOLOGY AND CONTROL OF EMERALD ASH BORER

EAB invasion is needed and could lead to practical 

and effective tactics to augment parasitism rates by 

these species. 

Considerable research has been conducted to 

identify semiochemical attractants or visual cues used 

by native and introduced EAB parasitoids including 

pheromones for T. planipennisi, and S. agrili and S. 

floridanus (Bauer et al., 2011, Cossé et al., 2012) and 

responses of P. sulcata, S. agrili, and S. floridanus 

to host kairomones associated with either EAB or 

ash trees (Roscoe et al., 2011, Johnson et al., 2014). 

Other research has addressed parasitoid response to 

visual stimuli including trap colors (Cooperband et 

al., 2013) and mechano-reception of vibrations by 

EAB larvae (Ulyshen et al., 2011). Further studies on 

olfactory, visual, and perhaps vibrational cues used 

by parasitoids to locate potential hosts may improve 

EAB biological control. Pre-release conditioning or 

oviposition manipulation with semiochemicals, for 

example, might increase parasitoid efficacy. Attractive 

lures or aerial application of volatile compounds 

could perhaps provide a means to attract or enhance 

parasitoid populations. 

Given the ongoing expansion of EAB, the 

economic costs resulting from urban infestations 

and the still unknown ecological ramifications of 

this invader for forest ecosystems, it seems clear that 

an integrated approach is needed to deal with EAB. 

Understanding and enhancing the collective effects of 

native and introduced parasitoids and predators on 

EAB will be crucial if native ash species are to persist 

in North America. 

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