Biological Control of Pests in Forests of Eastern United States

 

 

Emerald Ash Borer

Juli Gould, USDA-APHIS, Pest Survey, Detection, and Exclusion Laboratory, Otis ANGB, MA.  Juli.R.Gould@aphis.usda.gov

Leah Bauer, USDA-FS, Northern Research Station, East Lansing, MI.  lbauer@fs.fed.us

Range in North America

The emerald ash borer (EAB), Agrilus planipennis (Coleoptera: Buprestidae), (Figure 1) is an invasive wood boring beetle from Asia threatening North America’s ash trees (Fraxinus spp.).  It was introduced into the Detroit, MI area, probably during the 1990s, and was identified as the cause of ash mortality in southeastern Michigan in 2002 (Haack et al., 2002).  EAB is now considered established in urban and forested ecosystems throughout the lower peninsula of Michigan and contiguous areas of Ohio, Indiana, and Ontario, Canada; separate infestations also occur in the Upper Peninsula of Michigan, Illinois, and Maryland.  EAB appears well suited for climatic conditions in North America and destroys entire stands of ash.  It is predicted that EAB will continue to disperse along various continuous corridors of ash now present in natural and urban environments due to the widespread use of ash as a landscape tree (Federal Register, 2003). 

Damage

Fig. 2. Larva of the emerald ash borer (photo courtesy of David Cappaert, Michigan State University, www.forestryimages.org)

Fig. 3. Larval galleries of the emerald ash borer (photo courtesy of Art Wagner, USDA/APHIS/PPQ, www.forestryimages.org)

Fig. 4.  Dying ash trees in Plymouth, Michigan. 

EAB larvae (Fig. 2) feed on ash phloem (Fig. 3), cutting off nutrients and water, and resulting in tree death (Fig. 4) over a period of approximately four years.  Unlike other Agrilus species that are attracted to and attack mainly stressed trees, A. planipennis is able to attack and kill presumably healthy trees in both natural and urban settings.  As of 2006, managers estimate 25 million of Michigan’s 693 million ash trees have succumbed to EAB.  The risk that EAB poses to the remaining ash resource of the United States is substantial.  Twenty-two species of ash grow in the United States, of which sixteen species are native (USDA PLANTS database). There is increasing evidence that EAB will attack all Fraxinus spp., although innate susceptibility varies by species and variety (Liu et al., 2003; Wie et al., 2004; Rebek et al., 2006; Liu et al., in press).  Ash trees are present as ornamentals, street trees, and timber trees throughout the lower 48 states.  It is estimated that more than 7.5 billion ash trees are growing in U.S. timberlands, and unless climate restricts the distribution of EAB in parts of the U.S., these ash resources are considered at risk (USDA FS, 2007a).

Should EAB became established throughout the United States, the potential for adverse economic and environmental effects is extensive.  States that become infested will likely lose billions of dollars in forest products, and quarantines imposed by state and federal agencies may have dire consequences for plant and wood products industries.  White, black, and green ash are widespread species and important components of forested and riparian ecosystems throughout the northeastern United States and eastern Canada.  These three ash species comprise over 7% of all hardwood species and 5.5% of all species.  The wood is used for a variety of applications including tool handles, baseball bats, furniture, flooring, cabinetry, solid wood products, packing materials, pulp, paper, and basketry.   In addition to its ecological value in the ecosystem and economic value in the timber industry, ash has become an extremely popular urban/suburban landscape tree because of its aesthetic qualities, tolerance of less than ideal planting conditions, and resistance to gypsy moth and other pests.  In fact, ash is the most commonly planted tree in new residential, urban, and commercial environments.  The potential national impact of EAB on the urban environment alone is 0.5 to 2 % loss of total leaf area, or 30-90 million trees with a loss of $20-60 billion dollars.  In an initial economic analysis of EAB, the USDA Forest Service estimated that EAB, if not contained and eradicated, could cause approximately $7 billion in additional costs to state and local governments and landowners to remove and replace dead and dying ash trees in urban and suburban areas over the next 25 years.

Each Fraxinus spp. is adapted to slightly different habitats within forest ecosystems.  Several species are tolerant of poorly-drained sites and wet soils, protecting environmentally-sensitive riparian areas; e.g. pure stands of black ash grow in bogs and swamps in northern areas where they provide browse, thermal cover, and protection for wildlife such as deer and moose.  In agricultural and shelterbelt areas, ash provides vital shelter for livestock; e.g., ca. 25% of all trees in North Dakota are Fraxinus spp. Bark of young ash trees is a favored food of mammals including beaver, rabbit, and porcupines; older trees provide habitat for cavity-nesting birds such as wood ducks, woodpeckers, chickadees, and nuthatches; seeds are consumed by ducks, song and game birds, small mammals, and insects.

Native Natural Enemies

Studies conducted in Michigan since 2002 discovered four larval parasitoids attacking EAB, including three parasitoid species endemic to native Agrilus spp. and one exotic parasitoid species (Bauer et al., 2004, 2005; J. Gould unpublished); no egg parasitoids have been found to date (USDA FS 2007b).   Parasitism rates, however, are low (<1%) and clearly inadequate to suppress EAB populations (Bauer et al., 2005).  EAB parasitism rates in the U.S. are considerably lower than those reported in China (Liu et al., 2003; Yang et al., 2005) and those reported in the literature for native Agrilus spp.  Other natural enemies include entomopathogenic fungi, which cause ca. 2% mortality of EAB life stages under the bark.  Predaceous beetles and woodpeckers also attack EAB in Michigan.  The lack of natural enemies capable of suppressing EAB populations below a density threshold tolerable for survival of native ash trees is especially troubling (Federal Register, 2003) and this supports the need to introduce parasitoids that coevolved with EAB in Asia for biological control of EAB in North America (USDA FS, 2007b).

Biological Control Efforts

Emerald ash borer is reported from China, Mongolia, Japan, Korea, Russia, and Taiwan (Haack et al., 2002).  Since 2003, scientists have searched for EAB and its natural enemies in each of these countries except Taiwan.  Although the type specimen of A. planipennis is from Mongolia, Fraxinus and therefore EAB were not found in Mongolia.  Recent evidence suggests the type specimen was actually collected from Inner Mongolia in China (Schaefer, 2005).  In Japan, A. planipennis subsp. ulmi is reported from the four main islands, with a host range of ash, elm (Ulmus), walnut (Juglans), and wingnut (Pterocarya) (Haack et al., 2002).  Apparently EAB is rare and locally distributed in Japan, although a private collector secured a single EAB adult (Schaefer, 2005). In South Korea, EAB was found in 2005 and 2006 although no natural enemies were found (Williams et al., 2005; Bray et al., 2007).  In the Russian Far East, EAB was reared by Galina Yurchenko from Fraxinus rynchophylla, as were two species of braconids in the genus Spathius.   Collections are expected to continue in China and Russia in 2007, with the goal of finding additional EAB natural enemies. 

Foreign exploration for EAB natural enemies was more successful in China.  Since 2003, several parasitoids have been discovered in collaboration with scientists at the Chinese Academy of Forestry: Drs. Yang Zhong-qi and Zhao Tonghai and Professor Gao Ruitong (Liu et al., 2003; Bauer et al., 2005, 2006; Gould, 2006).  Surveys successfully located populations of EAB in Heilongjiang, Jilin, Lianoning, and Hebei Provinces, as well as in Beijing and Tianjin City (Liu et al., 2003,).  Genetically, EAB from North America are more similar to EAB collected in China than those collected in Korea or Japan (Bray et al., 2006, 2007).  In China, EAB is typically present at low density and is considered only a periodic pest of ash.  Populations are probably maintained at low density by a combination of factors including host plant resistance, climatic conditions, and natural enemies (Liu et al., in press). 

A new species of Spathius sp. (Hymenoptera: Braconidae) (Fig. 5) was found parasitizing EAB larvae in Jilin Province and Tianjin City (Liu and Liu. 2002; Liu et al., 2003, Yang et al., 2005).  This gregarious ectoparasitoid (Fig. 6) paralyzes EAB larvae and deposits from 1 to 20 eggs per larva.  The emergence of Spathius adults in the spring coincides with the presence of third- and fourth-instar EAB larvae, which are the preferred host stages.  This species has three to four generations per year in Tianjin, and up to 90% parasitism has been found in some ash stands (Yang et al., 2005). 

 

 

 

Fig. 5.  Female Spathius agrili ovipositing on EAB through ash bark (photo courtesy of Dr. Yang Zhong-qi, Chinese Academy of Forestry).

 

 

 

Fig. 6. Spathius agrili larvae consuming their EAB host (photo courtesy of Dr. Yang Zhong-qi, Chinese Academy of Forestry).

Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae) (Fig. 7) is a gregarious endoparasitoid of third- and fourth-instar EAB larvae discovered in Jilin and Liaoning provinces during 2003 (Liu et al., 2003).  It was described from subsequent collections in Heilongjiang province (Yang et al., 2006).  Field studies during 2005 in Jilin province revealed parasitism rates by T. planipennisi increased steadily from 8% in May to 40% in August (Liu et al., in press).  This parasitoid completes up to four generations per year and overwinters as larvae in host cadavers and galleries.  Parasitized EAB larvae produce an average of 35 parasitoids, with a range of 5 to 122 (Liu et al., in press).  The generation time for T. planipennisi reared at 25ºC in our USDA FS quarantine laboratory in Michigan is 20-25 days, and the sex ratio is 3.5 females to 1 male.  In the laboratory, the longevity of adults fed honey and water averages 24 days for females and 14 days for males (Liu and Bauer, 2007).

 

 

 

Fig. 7.  Tetrastichus planipennisi adult parasitizing EAB larva (photo courtesy of Dr. Leah Bauer).

Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae) (Fig. 8) is a solitary egg parasitoid discovered parasitizing A. planipennis eggs on ash trees in Jilin province in 2004 (Zhang et al., 2005).  Field studies in 2005 revealed O. agrili completes at least two generations per year, with the highest rates of parasitism, averaging ca. 60%, during July and August (Liu et al., in press).  Although O. agrili is parthenogenic (females produce females without mating), field collections in China demonstrate a female-biased sex ratio of 15:1.  O. agrili overwinters as mature larvae in A. planipennis eggs, and the majority of individuals do not emerge until summer, during peak oviposition period for A. planipennis.  The generation time for O. agrili reared at 25ºC in the USDA FS quarantine laboratory in Michigan was 20-25 days, and adult females fed honey and water lived an average of 14 days.  O. agrili prefers to oviposit in A. planipennis eggs ranging from newly laid to 9-days-old.  Females parasitize an average of 24 A. planipennis eggs during their lifetime, with a daily maximum of five and a lifetime maximum of 62 (Bauer and Liu, 2007).

 

 

 

Fig. 8.  Oobius agrili adult parasitizing EAB egg (photo courtesy of Dr. Leah Bauer).

 

An undetermined species of Sclerodermus sp. (Hymenopetera: Bethylidae) attacks EAB pre-pupae, but parasitism levels are low.  Female parasitoids enter overwintering chambers of EAB pre-pupae, remove frass, and deposit 15-20 eggs; ca. 70% of females are wingless causing them to have only a very limited dispersal capability.  Members of this genus have also been known to sting humans, making this species an unsuitable biocontrol agent.

Predicting the potential for successful biological control of EAB cannot be done by reference to prior biocontrol success against other buprestids because no other species of such borers have targets for biological control (Gould et al., 2005).  However, it is probable that one or more of the EAB natural enemies found recently in China will be useful biocontrol agents in North America based on the biological characteristics of the species being considered for release.  Kimberling (2004) reviewed characteristics of successful biological control agents and found that the most important traits are that the species is 1) a parasitoid, 2) multivoltine, and 3) monophagous.  The Spathius, Oobius, and Tetrastichus species attacking EAB fit this profile (Table 1), also having female-biased sex ratio, oviposition in or on its host, and a multivoltine life history. While only Tetrastichus is strictly monophagous, the other two species prefer EAB as a host. 

Table 1.  The characteristics of EAB parasitoids, and how they relate to the likelihood of successful biological control.

Characteristic

Probability for Biocontrol Success Higher

Spathius

Tetrastichus

Oobius

Predator vs. Parasitoid

Parasitoid

Yes

Yes

Yes

# Generations per year

> 1 compared to host

3-4

3-4

2

Polyphagy

Monophagous

Prefers EAB

Yes

Prefers EAB

Sex Ratio (F:M)

More Females

3:1

2.5:1

15:1

Oviposition Location

Oviposition in or on host

Yes

Yes

Yes

Internal Feeder?

Internal Feeder

No

Yes

Yes

Current Status

Research in 2006 concentrated on developing methods to rear the parasitoids in the laboratory and conducting host specificity tests to predict non-target effects. Methods to rear Spathius, Tetrastichus, and Oobius throughout the year in the laboratory have been developed.  Spathius and Tetrastichus can be reared in EAB larvae dissected from infested ash logs or raised on artificial diet, then implanted in small ash branches.  Oobius can be reared on EAB eggs produced in the laboratory from EAB adults reared from infested ash logs harvested in the field.  Research is ongoing to maximize parasitoid production and optimize methods to stockpile parasitoids in cold storage for later release. 

Host specificity testing has been completed for all three parasitoids.  In laboratory no-choice assays, T. planipennisi did not parasitize the following wood-boring insect larvae implanted in small branches of their respective host plants:  8 species of Buprestidae (Agrilus anxius, A. bilineatus, A. ruficollis, A. subcinctus, A. putillus?, Chrysobothris femorata, C. floricola, C. sexsignata); 5 species of Cerambycidae (Neoclytus acuminatus, Megacyllene robiniae, Astylopsis sexguttata, Monochamus scutellatus, unknown sp. in maple); and one cephid sawfly species (Janus abbreviatus).  We also tested larvae of one tenebrionid beetle (Tenebrio molitor) and two species of Lepidoptera (Galleria mellonella, Manduca sexta) by implantation in small ash branches; Manduca sexta larvae were also tested by exposure on tomato leaves.  Tetrastichus rejected all species as hosts except actively-feeding EAB larvae implanted in ash branches.  These assays provide strong evidence that Tetrastichus is host specific.   Surveys of 2,072 Agrilus spp. (other than EAB) larvae from China did not reveal any parasitism by T. planipennisi.

Spathius  agrili exhibited some oviposition on other species in the genus Agrilus (A. bilineatus, A. anxius, A. zanthoxylumi, A. mali, and A. inamoenus); however, the percentage of larvae attacked was significantly lower than on EAB.  Spathius did not parasitize several of the Agrilus species tested (A. auriventris, A. auriventris A. sorocinus, A. lewisiellus), other wood boring beetles (Buprestidae, Cerambycidae), or wood-boring Lepidoptera (Pyralidae, Cossidae, and Carposinidae).  Olfactometer studies revealed that female S. agrili was only attracted to leaves of ash and willow; they were not attracted to 11 other host plants of other common wood-boring insects.  Surveys of 2,072 Agrilus spp. larvae (not EAB) from China did not reveal parasitism by S. agrili

Laboratory no-choice and choice assays were performed for O. agrilis.  In the no-choice assays, Oobius were exposed to eggs of the following wood-boring insects laid on their respective host plants:  six species of Buprestidae (Agrilus anxius, A. bilineatus, A. cyanescens, A. egenus, A. ruficollis A. subcinctus,) and two species of Cerambycidae (Megacyllene robiniae, Neoclytus acuminatus).  We also assayed eggs of four species of Lepidoptera laid on small ash branches (Bombyx mori, Choristoneura rosaceana, Manduca sexta, Pieris rapae).  Oobius did not parasitize eggs of Cerambycidae, Lepidoptera, or eggs of the smaller Agrilus spp.:  A. cyanescens, A. subcinctus, and A. egenus.  Eggs of the larger Agrilus spp. (A. anxius, A. bilineatus, A. ruficollis) were parasitized.  Unacceptable Agrilus eggs are about half the size of acceptable Agrilus eggs, suggesting Agrilus egg size may be a limited factor for Oobius.  In the choice assays, Oobius were exposed to EAB eggs and eggs of the three larger Agrilus spp. accepted during no-choice assays (A. anxius, A. bilineatis, or A. ruficollis).  When given a choice, Oobius demonstrated a strong preference for EAB eggs on ash vs. eggs of either of the other species on their respective host plants (birch, oak, or raspberry, respectively).  These results suggest that Oobius has a strong affinity for ash trees and anything more than incidental parasitism of native Agrilus spp is highly unlikely.  

Applications for permits for field release of Spathius, Tetrastichus, and Oobius were submitted in January of 2007.  If permits are approved, field release is anticipated in the summer of 2007.

References

Bauer, L. S., H-P. Liu, R. A. Haack, T. R. Petrice, and D. L. Miller.  2004.  Natural enemies of emerald ash borer in southeastern Michigan, p. 33.  In: Anon. Proceedings of the 2003 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Service FHTET 2004-02.

Bauer, L. S., H-P. Liu, R. A. Haack, T. R. Petrice, and D. L. Miller. 2005. Emerald ash borer natural enemy surveys in Michigan and China, pp. 71-72. In: Anon Proceedings of the 2004 Emerald Ash Borer Research and Technology Development Meeting, Romulus, MI. USDA FS FHTET-2004-15.

Bauer L. S., H-P Liu, R-T Gao, and T-H Zhao.  2006.  Egg and larval parasitoids of emerald ash borer from China:  potential for biocontrol in North America, pp. 48-49. In Anon. Proceedings of the 2005 Emerald Ash Borer Research and Technology Development Meeting.  FHTET-2005-16.

Bauer, L. S. and H-P. Liu.  2007. Oobius agrili (Hymenoptera: Encyrtidae), a solitary egg parasitoid of emerald ash borer from China, pp. 63-64.  In: Anon. Proceedings of the 2006 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Service FHTET-2007-04.

Bray, A. M., L. S. Bauer, R. A. Haack, T. M. Poland, and J. J. Smith. 2006. Invasion genetics of emerald ash borer (Agrilus planipennis Fairmaire) in North America, pp. 5-6.  In: Anon. Proceedings of the 2006 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Service FHTET-2005-16.

Bray, A. M., L. S. Bauer, R. W. Fuester, H-Y. Choo, D-W. Lee, N. Kamata, and J. J. Smith.  2007. Expanded explorations for emerald ash borer in Asia and implications for genetic analysis, pp. 6-7.  In: Anon. Proceedings of the 2006 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Service FHTET-2007-04.

Federal Register. 2003.  Emerald ash borer: Quarantine and Regulations. 7 CFR Part 301 [Docket No. 02-125-1]

Gould, J. R. 2006.  Progress on collecting, studying, and rearing parasitoids of emerald ash borer from China, p. 50.  In: Anon. Proceedings of the 2005 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Service FHTET-2005-16.

Gould, J., L. Bauer, H-P Liu, D. Williams, P. Schaefer, and D. Reardon.  2005.  Potential for biological control of the emerald ash borer.  In: Anon. Proceedings of the USDA Interagency Research Forum on Gypsy Moth and other Invasive Species.  Annapolis, Maryland,. January 2005.

Haack, R. A., E. Jendek, H-P. Liu, T. Petrice, T. M. Poland, and H. Ye. 2002.  The emerald ash borer: a new exotic pest in North America. Michigan Entomological Society Newsletter 47: 1-5.

Kimberling, D. N. 2004.  Lessons from history: predicting successes and risks of intentional introductions for arthropod biological control.  Biological Invasions 6: 301-318.

Liu, H-P. and L. S. Bauer.  2007. Tetrastichus planipennisi (Hymenoptera: Eulophidae), a gregarious larval endoparasitoid of emerald ash borer from China, pp. 61-62.In Anon. Proceedings of the 2006 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Service FHTET-2007-04.

Liu, H-P, L. S. Bauer, R-T. Gao, T-H. Zhao, T. R. Petrice, and R. A. 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.

Liu, H-P, L. S. Bauer, D. L. Miller, L-W. Song, Q-S. Luan, S-H. Sun, and R.Z. Jin.  Seasonal abundance and population dynamics of Agrilus planipennis (Coleoptera: Buprestidae) and its natural enemies Oobius agrili (Hymenoptera: Encyrtidae) and Tetrastichus planipennisi (Hymenoptera: Eulophidae) in China.  Biological Control  In press.

Liu, G-J. and E-S. Liu. 2002. Preliminary report on control of emerald ash borer. An internal report of Ornamental Tree Management of Guangang Area, Tianjin, China.

Rebek, E., D. Herms, D. Smitley, P. Bonello, and D. Cipollini. 2006. Interspecific variation in ash resistance to emerald ash borer, p. 17.  In: Anon. Proceedings of the 2005 Emerald Ash Borer Research and Technology Development Meeting. FHTET-2005-16.

Schaefer, P. W. 2005. Foreign exploration for emerald ash borer and its natural enemies, pp 67-68.  In: Anon. Proceedings of the 2005 Emerald Ash Borer Research and Technology Development Meeting. FHTET-2004-15.

USDA FS. 2007a.  Effects of urban forests and their management on human health and environmental quality. http://www.fs.fed.us/ne/syracuse/Data/Nation/data_list_eab.htm

USDA FS. 2007b. Emerald ash borer natural enemies.  http://ncrs.fs.fed.us/4501/eab/current/enemies/

Wie, X., D. Reardon, Y. Wu, J-H. Sun.  2004.  Emerald ash borer, Agrilus planipennis, in China:  a review and distribution survey.  Acta Entomologica Sinica 47: 679-685.

Williams, D., H-P., and Y-S. Jo.  2005.  Exploration for emerald ash borer and its natural enemies in South Korea during May-June 2005, p. 52.  In: Anon. Proceedings of the 2005 Emerald Ash Borer Research and Technology Development Meeting. USDA Forest Service FHTET-2005-16.

Yang, Z-Q, J. S. Strazanac, P. M. Marsh, C. van Achterberg, and W-Y. Choi.  2005.  First recorded parasitoid from China of Agrilus planipennis: A new species of Spathius (Hymenoptera: Braconidae, Doryctinae).  Annals of the Entomological Socoiety of America 98: 636-642.

Yang, Z-Q., J. S. Strazanac, Y-X. Yao, and X-Y. Wang. 2006. A new species of emerald ash borer parasitoid from China belonging to the genus Tetrastichus Haliday (Hymenoptera: Eulophidae) parasitizing emerald ash borer from China. Proceedings of the Entomological Society of Washington. 108: 550-558.

Zhang, Y-Z., D-W. Huang, T-H. Zhao, H-P. Liu, and L. S. Bauer. 2005.  Two new egg parasitoids (Hymenoptera: Encyrtidae) of economic importance from China. Phytoparasitica 33: 253-260.