Biological Control of the Emerald Ash Borer
In 2002, the emerald ash borer (EAB), Agrilus planipennis(Coleoptera: Buprestidae), an Asian beetle that feeds on ash trees (Fraxinus spp.), was discovered as the cause of widespread ash tree mortality in southeastern Michigan and nearby Windsor, Ontario. Evidence shows that EAB was introduced to Michigan during the early 1990s by transport of infested solid-wood packing materials from China. Despite eradication efforts by regulatory agencies in the U.S. and Canada, EAB is now considered established throughout much of Michigan and areas of Illinois Indiana, Ohio, Pennsylvania, and Ontario, Canada. Outlier infestations are known in Maryland, Missouri, Virginia, West Virginia, Wisconsin, and Quebec, Canada. Long-distance movement of EAB is generally caused by people transporting infested ash firewood, nursery stock, timber, and manufactured goods, as well as the abundance of ash in eastern and northern forests and its extensive use in landscaping, will result in the continued spread of EAB in North America.
The presence of EAB in North America puts Nearctic Fraxinus spp. at risk. Those endemic to the northern hardwood forests include white ash (F. americana), green ash (F. pennsylvanica), and black ash (F. nigra) trees, and the less common blue ash (F. quadrangulata) and pumpkin ash (F. profunda). Each species is adapted to different sites in our forests, serving as critical ecological resources, particularly in riparian zones. Ash trees are also important economically with 8 billion ash trees on U.S. timberlands valued at $282.25 billion (USDA FS FIA). Moreover, ash trees are one of the most prevalent trees in urban areas, agricultural lands, and shelterbelts and the costs to communities and landowners for removal and replacement will continue to escalate. The 2003 Federal Register reported costs of ash removal and replacement at $11.7 billion for six infested southeastern Michigan counties alone. Clearly, methods to slow the spread and control EAB in North America are needed. Although some systemic insecticides are beginning to show promise for the protection of high-value ash trees, sustainable management methods are needed for ash in forested and riparian ecosystems.
Biological control is a long-term management strategy accepted throughout the world for the sustained control of invasive insects. This approach is used for non-native species that 1) have been established for more than 5 years, 2) cannot be eradicated and 3) cause significant ecological or economic damage. Biological control involves research in the insect’s country of origin to find, isolate, and identify its natural enemies, ranging from parasites to predators to pathogens. In the U.S., permits for release of highly host-specific natural enemies or “biocontrol agents” may be granted by USDA APHIS PPQ after completion of extensive research on the biology of both the host and its natural enemies in the U.S. and in the country of origin, risk benefit analyses, public comment, and state concurrence.
Over the years, regulatory agencies have determined EAB eradication efforts ineffective and quarantine compliance incomplete. Land managers are now seeking sustainable methods such as biological and microbial control for managing EAB populations. Since 2002, we have been working to develop an EAB biological control program in the U.S., which includes research in the U.S. and China. Below is a brief summary of our progress.
Natural Enemies of EAB in Michigan & China: EAB is native to countries in northeastern Asia including China, Korea, the Russian Far East, and Japan, where it is considered a minor and periodic pest of ash trees. For this reason, only minimal literature was available on EAB when it was discovered in Michigan in 2002. Soon after the discovery of EAB in N.A., we began studying its biology, natural enemies, and population dynamics in Michigan and China through collaborations with scientists at Michigan State University (MSU) and the Chinese Academy of Forestry (CAF). We also initiated research with MSU to determine the country of origin for EAB in North America using comparative molecular genetics.
Our EAB natural enemy research started in 2002 in parks southeast Michigan where EAB populations were sampled for natural enemies commonly associated with wood-boring insects: predaceous and parasitic insects, insect-pathogenic fungi, and woodpeckers. By 2004, we had expanded this study to include a total of 17 EAB-infested areas of southeast Michigan.
In China, EAB outbreaks were previously reported in native and N.A. ash species, including F. americana and F. pennsylvanica, planted in Heilongjiang and Shandong provinces. More recent EAB outbreaks were reported in the Tianjin in plantings of F. velutina, an ash species endemic to the southwestern U.S. and northern Mexico. To locate research sites in China, we sampled ash trees in 2003 for EAB and natural enemies in the provinces or cities of Heilongjiang, Jilin, Liaoning, Hebei, Tianjin, and Shandong. During this initial survey, and in a subsequent study in 2004, Spathius agrili and two parasitoid species previously unknown to science were found attacking EAB at field sites in China.
The use of biological and microbial control agents in North America is expected to suppress EAB densities below a tolerance threshold for native ash trees. If successful, our native ash species will continue to help sustain healthy forests, woodlots, and riparian areas.
EAB Natural Enemy Research in Michigan:
Predators. In 2003 and 2004, we studied natural enemies attacking EAB in southeastern Michigan. The most conspicuous natural enemies of immature EAB in were the downy, Picoides pubescens, hairy, P. villosus, and red-bellied, Melanerpes carolinus, woodpeckers. Based on analyses of infested ash trees felled during our study, we estimated woodpeckers consumed an average of 16% of EAB larvae and pupae at our field sites from 2002-2004. Other predators included the larvae and adults of three beetle species that live under tree bark and feed on EAB in infested ash trees: Enoclerus sp. (Cleridae), Catagenus rufus F. (Passandridae), and Tenebroides sp. (Trogossitidae).
Parasitoids. Six hymenopterans have been reared and confirmed as ectoparasitoids of immature EAB. During our Michigan natural enemy study were: Atanycolus hicoriae, A. simplex (Braconidae), Phasgonophora sulcata (Chalcididae), Spathius floridanus, and one non-native ectoparasitoid, Balcha indica (Eupelmidae). Another parasitoid, reared from EAB-infested logs during our Michigan study, Dolichomitus sp. (Ichneumonidae), was recently confirmed as an EAB larval endoparasitoid by Dr. Jian Duan, ARS, Newark, DE during his recent natural enemy research in Pennsylvania. Combined larval parasitism from these parasitic wasps, however, accounted for <0.5% EAB mortality. No egg parasitoids emerged from >6000 EAB eggs collected and reared, however, we find incomplete development of unknown egg parasitoid(s), as evidenced by the occasional partially-developed pupa inside EAB eggs.
Since completion of this early work on EAB natural enemies, MSU collaborators have found high levels of parasitism by A. hicorae, an incidental larval ectoparasitoid of EAB, in a heavily-infested state park north of the Detroit area. We are now collaborating with MSU and FS to develop a rearing method for this parasitic wasp. Other scientists in the U.S. and Canada are beginning to study EAB natural enemies, and are finding P. sulcata and B. indica also reach high levels in some sites. High prevalence of these parasitoids, however, tends to occur in stands where the majority of the ash trees have already died.
Pathogenic fungi. On average, mortality from insect-pathogenic fungi was about 1% of EAB dissected from ash trees sampled during our natural enemy studies, including isolates of Beauveria bassiana, Lecanicillium lecanii, Metarhizium anisopliae, Paecilomyces farinosus, and P. fumosoroseus. Interestingly, most of these fungi were isolated from single field site where a fungal epizootic resulted in about 62% mortality of EAB larvae, pupae, and emerging adults.
Nematodes in EAB. Research to understand factors affecting EAB fecundity and fertility in the laboratory, we periodically find nematodes within the hemocoel of EAB adults reared from Michigan. Nematodes were isolated and sent to Dr. Robin Giblin-Davis at the University of Florida. Using comparative molecular genetics, he identified them as the free-living stage of a tylenchid nematode, which feed on fungi in the galleries of wood-boring insects. The effect of these nematodes on EAB is unknown.
Other causes of EAB mortality. Overcrowding of EAB larvae in ash trunks frequently results in high larval mortality due to starvation – they simply run out of phloem. Under the circumstances, we often find it surprising that larval cannibalism is minimal, tending to occur occasionally when one larva feeds across another larva in a separate gallery.
EAB Natural Enemy Research in China:
Ash, EAB, and natural enemies. In 2003, we sampled ash plantings for EAB and its natural enemies in natural areas, parks, plantations, along streets and highways in cities and in rural areas. We sampled F. chinensis (F. rhynchophylla) and F. mandshurica, which are native to China, and F. pennsylvanica and F. velutina, which are native to North America. We found EAB or old galleries in Heilongjiang, Jilin, Liaoning, Hebei, Beijing, and Tianjin provinces. Prior to this, EAB had been reported in Heilongjiang, Shandong, and Tianjin provinces, thus our work expanded the distribution of EAB in China and increased the probably of finding EAB natural enemies. Our survey sites in Shandong province were limited to ash trees in Binzhou city, thus additional sampling in the province might identify historical EAB sites. As found and reported earlier in China, nearctic ash species are more susceptible to EAB than were the native species. Of the native species, F. chinensis was more resistant than F. mandshurica.
Parasitoids. In 2003 at sites in Jilin province, we discovered a previously unknown eulophid endoparasitoid of EAB larvae, which was later named Tetrastichus planipennisi. During research in Jilin province in 2004, we discovered an encyrtid egg parasitoid, which we named Oobius agrili. The previously known parasitoid, Spathius agrili, was also reared from EAB although less frequently in the northern provinces.
Initially, we focused our research effort on the population biology of EAB infesting F. pennsylvanica, planted in a park in Jilin province, where the two new EAB parasitoids, O. agrili and T. planipennisi, overlap in distribution. We estimated that combined parasitism by these two natural enemies resulted in 74% population reduction of EAB at this site in 2005. The F. pennsylvanica trees, although infested with EAB since they were planted about 30 years ago, remain live and produce seeds.
During the course of this study, we also studied the biology of these two EAB parasitoids. We found that O. agrili goes into obligate diapause during August as a mature larva inside EAB eggs. It remains in diapause until the following June, when another generation of EAB eggs are laid, thus completing about two generations per year. T. planipennisi survives the winter as mature larvae in EAB galleries. They complete development during early spring, emerge, and continue to parasitize overwintering EAB larvae, thus completing at least four generations per year.
Developing a Biological Control Program in the U.S. for EAB:
Parasitoid biology, rearing, and host specificity. Since 2004, we have been rearing O. agrili and T. planipennisi from EAB eggs and larvae sampled from ash trees in China and shipped to our quarantine laboratory in Michigan. These are used to study parasitoid prevalence in China, EAB and parasitoid biology, host specificity, and develop laboratory rearing methods. Similar research on S. agrili, the third EAB parasitoid, has been done in quarantine by scientists at APHIS.
Release of EAB parasitoids. By 2007, much of the laboratory research on these three EAB parasitoids was completed, and we submitted permit requests to APHIS PPQ for their environmental release in Michigan. This involved working closely with APHIS to prepare the Environmental Assessment (EA). The EA requesting permission to release was posted on the Federal Register for a 60-day public comment period. After a finding of no significant impact (FONSI) and state concurrence, release permits were issued and parasitoid releases began at the end of July 2007 in Michigan. This information is available at: Emerald Ash Borer; Availability of an Environmental Assessment
In summer and fall 2007, we released O. agrili and T. planipennisi each at two research sites, and APHIS released S. agrili at three different sites. In 2008, additional research sites were set up in central Michigan, and two each in Indiana and Ohio. In 2009, study sites were set up in Maryland and Illinois.
Establishment of EAB parasitoids. Early in the spring of 2008, we successfully recovered O. agrili from one of our 2007 release sites and APHIS recovered S. agrili at one of their sites. In 2009, in collaboration with scientists from Michigan State University, University of Massachusetts, USDA ARS, and USDA APHIS, both T. planipennisi and O. agrili were recovered and presumed established at three of our Michigan research sites; successful recovery of S. agrili at these sites cannot be confirmed until adults emerge from cocoons and are identified.
Recording and monitoring biocontrol sites. To create a permanent record of each release site, each release site is mapped using GIS. The efficacy of biocontrol agents in reducing ash decline or mortality is being evaluated by are monitoring the health of 50 ash trees at each release site and a nearby control site, where no parasitoids were released. Depending on the initial healthy of ash trees in the stand, history of EAB infestation, weather, and other factors, this will likely take several years. In 2008, we also initiated EAB life table studies to quantify stage-specific mortality factors at release sites where the three parasitoid species were released.
EAB Biological Control Laboratory. To centralize and increase the efficiency of EAB parasitoid rearings, APHIS and FS are working together to develop an EAB Biological Control Program. APHIS recently completed construction of a parasitoid mass-rearing laboratory in Brighton, MI. Once new personnel are hired, we will begin training them to rear EAB, F.&mnsp;uhdei in the greenhouse, O. agrili, and T. planipennisi.
Liu HP, LS Bauer, DL Miller, TH Zhao, RT Gao, LW Song, QS Luan, RZ Jin, CQ Gao. 2007. Seasonal abundance of Agrilus planipennis (Coleoptera: Buprestidae) and its natural enemies Oobius agrili (Hymenoptera: Encyrtidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae) in China. Biological Control 42: 61-71.
Zhang YZ, DW Huang, TH Zhao, HP Liu, LS Bauer. 2005. Two new species of egg parasitoids (Hymenoptera: Encyrtidae) of wood-boring beetle pests from China. Phytoparasitica 53: 253-260.
Liu HP, LS Bauer, RT Gao, TH Zhao, TR Petrice, RA Haack. 2003. Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Great Lakes Entomologist 36: 191-204.
EAB Biological Control Methods
Bauer, Leah; Hansen, Jason; Gould, Juli. 2014. Yellow Pan Traps: A Simple Method for Trapping Larval Parasitoids Released for Biological Control of the Emerald Ash Borer. 3 p. (pdf - You may obtain a free PDF reader from Adobe.)
Gould, Juli S.; Bauer, Leah S.; Lelito, Jonathon; Duan, Jian. 2013. Emerald ash borer biological control release and recovery guidelines. 2013. Riverdale, MD: U.S. Department of Agriculture, Animal Plant Health Inspection Service [and other USDA and state agencies]. 43 p.
Duan, Jian J.; Bauer, Leah S.; Ulyshen, Michael D.; Gould, Juli R.; Van Driesche, Roy. 2011. Development of methods for the field evaluation of Oobius agrili (Hymenoptera: Encyrtidae) in North America, a newly introduced egg parasitoid of the emerald ash borer (Coleoptera: Buprestidae). Biological Control. 56: 170-174.
- Leah S. Bauer, US Forest Service, Northern Research Station Research Entomologist
- Juli Gould, USDA APHIS, CPHST
- Jian Duan, USDA ARS BIIRU
- Deborah McCullough, Michigan State University
- Tonghai Zhao, Chinese Academy of Forestry
- Cliff Sadof, Purdue University
- Roy Van Driesche, University of Massachusetts
- Richard Reardon, USDA FS FHTET
- Jonathan Lelito, USDA APHIS
Last Modified: 12/10/2014