A department of the College of Agriculture and Life Sciences at Cornell University

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Ann E. Hajek Professor Department of Entomology 6126 Comstock Hall Ithaca, New York 14853-0901 607-254-4902 (lab 4992) fax: 607-255-0939 aeh4@cornell.edu

Education:

Ph.D. - University of California, Berkley, 1984
M.S. - University of California, Berkeley, 1980
B.S. - University of California, Berkeley, 1974

Appointment: Research 60%, Teaching - 40%

Areas of Specialization: Insect pathology, Biological control

Teaching Activities

Entom 277 – Natural Enemies: An Introduction to Biological Control (every other year; odd springs)
An introduction to the dynamic field of biological control. What is it and when should it be used? This course covers a diversity of types of biological control including use of parasitoids, predators, pathogens, and competitors as well as plant breeding to control pests from microbes to weeds to invertebrates and vertebrates. This course is intended for students curious about safely controlling pests.

Entom 463 – Invertebrate Pathology (every other year; even springs)
Lectures present principles of pathology as applied to invertebrates. Topics explored include noninfectious and infectious diseases caused by viruses, bacteria, fungi, protozoa, and nematodes, epizootiology of insect diseases, and use of pathogens for control. Laboratories include a diversity of pathogens and hosts using techniques such as microinjection, electrophoresis, immunoassay, density gradient centrifugation, soil extraction, and computer simulation.

Entom 477 – Biological Control (co-taught with Jan Nyrop) (every other year; odd falls)
Lectures present case studies exploring classical biological control, augmentation and conservation, and applications of strategies to control arthropods and weeds. Labs focus on selected concepts in more depth using live organisms.

Entom 670 – Seminar on Biological Control (falls)
This is an upper level seminar in biological control, each season covering a theme chosen by participating students and faculty. The format consists of weekly discussion groups with each participant presenting at least one oral report based on independent reading or research focussing on a central theme for the semester.

Research Interests:

Research Interests and Projects Currently Underway

Interests in our laboratory are multi-faceted, with questions ranging from molecular to cellular to organismal levels. Much of our work has focused on fungal diseases of insects associated with trees (especially lepidopteran larvae and coleopteran adults), but studies in the laboratory are not restricted to these groups or this habitat. Major long-term research interests are listed below:

I. Epizootiology of insect diseases

Epizootiology has been a primary focus of research in our laboratory, with explorations targeting many different aspects over the years. The model system that we have examined most extensively has been gypsy moth and the fungal pathogen Entomophaga maimaiga. Gypsy moth is an outbreak species that was introduced to North America from Europe in 1868-69 but is native across temperate Europe and Asia. Entomophaga maimaiga (Zygomycetes: Entomophthorales) was first found infecting gypsy moth in North America in 1989 and has since then spread on its own and with a little help, causing high levels of infection in both high and low density gypsy moth populations. As a result, many credit E. maimaiga with now being the principal natural enemy in North America--responsible for crashes in outbreak gypsy moth populations. Included in our years of studies have been spatial and temporal variability in host and pathogen and dynamics of host/pathogen interactions. On an ecological level, interactions of host and pathogen with the environment (e.g., host tree species, weather, types of soils, etc.) have been, and are presently being, explored. For a fairly recent review of many of our studies see Hajek, 1999, Microbiol. Molec. Biol. Rev.

II. Evolution of pathogen virulence and host resistance/population structure of pathogens

Questions about the evolution of pathogen virulence are on the minds of many people with recent episodes of ?new? diseases such as SARS, mad cow disease, Ebola virus and hantavirus, to name a few. The poxvirus causing myxomatosis in rabbits is well known as providing an example of coevolution between European rabbits and a South American rabbit poxvirus, with virulence of the virus decreasing through time as rabbit resistance increased. Pathogens of insects provide excellent model systems for further studies of host/pathogen interactions to better understand changes in pathogen virulence and host resistance. Insect pathogens range from those killing hosts quickly to those causing chronic disease and include microbes in the same major groups that cause diseases in plants and other animals (viruses, bacteria, fungi, protists). We have been interested in studying some of the most virulent insect pathogens and asking questions about variability in virulence and change in virulence through time. Along with these studies go studies of population structure of pathogens to better understand the genotypic variability. At present, studies on this subject focus on gypsy moth and E. maimaiga, investigating the population genetics of this entomophthoralean fungus as well as resistance to E. maimaiga in geographic strains within the gypsy moth species.

III. Host specificity of insect pathogens/Non-target effects of biological control

Our research has focused on those factors determining host specificity of insect pathogenic fungi, principally using the gypsy moth and Entomophaga maimaiga as a model system. When a caterpillar is a non-host, is this fungus unable to penetrate the cuticle (to infect) or is the fungus unable to survive once within the host? Studies of the activity of fungal spores on gypsy moth cuticle using electron microscopy yielded the interesting findings that a group of cuculliine noctuids (a subgroup of owlet moths, a common family of moths in northeastern U.S. forests) have a mucilaginous layer covering their cuticles that prevents spore attachment. In addition, exciting results from studies by Claudia Lopez Lastra, a visiting Argentine scientist working in our laboratory, demonstrated differential immune responses by gypsy moth to E. maimaiga (a successful pathogen) and Entomophaga aulicae, a closely related species in the Entomophthorales that cannot successfully develop within gypsy moth.

Along with basic studies of host specificity, we conducted ecological studies to evaluate the differences between infection in the laboratory and infection occurring in the field. In the most recent study, over 5 years in Virginia and West Virginia with Linda Butler and John Strazanac (West Virginia University), we have found that E. maimaiga rarely infects insects other than gypsy moth. During laboratory bioassays, the most susceptible group besides gypsy moth are native tussock moths (the same family as gypsy moth) but only low percentages were found infected in 2 out of 5 years of field collections, when high levels of infection among the gypsy moth larvae occurred. Our results have added to the information helping to develop methods to ensure that biological control practices are environmentally safe.

IV. Biological control, especially using insect pathogens

Work in our laboratory has focused on biological control of invasive species but is not solely restricted to those pests. Also, we have principally worked with fungal pathogens. There are over 700 species of fungal pathogens infecting insects and mites and several of these have been developed as microbial insecticides in numerous countries. We have conducted studies with how to preserve fungal pathogens, how to grow them inside and outside of hosts to produce specific fungal stages, and how to apply them in the field for pest control.

At present, we have been focusing on use of fungal pathogens to control the invasive Asian longhorned beetle (now in New York City and Long Island, Chicago, Toronto and two areas in New Jersey). We are working with Hyphomycetes and a novel application method that was originally developed in Japan for control of a closely related beetle. Non-woven fiber bands containing cultures of insect pathogenic Hyphomycetes are placed around tree trunks where adult Asian longhorned beetles contact them when wandering during their normal prematurational development period. Lab and field studies are demonstrating that this application method is effective and the persistence of activity of fungi in these bands shows that this method has great potential against these long-lived beetles.

Fungi in the Entomophthorales can be virulent pathogens, causing rapid epizootics in host populations, but they have seldom been exploited for control, in part because they are difficult to mass produce and apply successfully for control. Our studies have shown that E. maimaiga resting spores are the best stage to release for gypsy moth control and we can produce these spores within hosts or in culture media. At present, we are conducting studies on resting spore dormancy to develop methods to make sure that resting spores being released for gypsy moth control will germinate that season.

Our laboratory frequently investigates new topics for research. Recently, we have been finding that the fungal pathogens already occurring in North America can infect enough soybean aphids so that insecticidal control is not necessary. Additional interests in our laboratory include non-occluded viral diseases of butterfly and hawk moth larvae that can cause major crashes among insects used by researchers and/or ?butterfly houses?. We are also interested in the general diversity of entomophthoralean fungi, especially species infecting Lepidoptera and Diptera.

Postdoctoral, Graduate and Undergraduate Student Research Projects

Charlotte Nielsen, a postdoc in the laboratory, is presently addressing questions about population genetics of the gypsy moth fungal pathogen Entomophaga maimaiga as well as evolution of virulence of this pathogen.

Undergraduate and graduate students are involved in a diversity of projects related to insect pathogens. James Reilly is presently working on phenotypic plasticity in virulence of baculoviruses infecting caterpillars. Jen Lund is working on effects of Hyphomycete fungi on reproduction by the invasive Asian longhorned beetle.  Josh Hannam has been conducting studies on fungal pathogens infecting soybean aphids.

Thomas Dubois completed his Ph.D. in 2003, studying use of Hyphomycete fungi to control Asian longhorned beetle, conducting field studies in China for several seasons. He explored use of non-woven fiber bands impregnated with cultures of entomopathogenic fungi (a novel application method) with great success.

Melanie Filotas completed her Ph.D. in 2002, studying biology and epizootiology of a fungal pathogen of forest tent caterpillar, including basic biological studies of host/pathogen interactions with this little-known pathogen.

Italo Delalibera Jr.  completed his Ph.D. in 2002 studying a fungal pathogen infecting cassava green mite, that was introduced from Brazil to central Africa for control of this serious cassava pest. Italo developed a method for culturing this fastidious pathogen, conducted studies of host specificity, learning that this pathogen is a new species, which he described.

Graduate student projects could focus on any aspects of the biology, epizootiology and evolution of microbes, especially pathogenic microbes, and entomopathogenic nematodes, associated with insects as well as insect responses to these natural enemies, from behavioral to immunological.

Lab Members:

Visiting Scientist
Claudia Lopez Lastra (ccl2@cornell.edu)

Graduate Students
Italo Delalibera (id24@cornell.edu)
Thomas Dubois (tld11@cornell.edu)
Melanie Filotas (mjf23@cornell.edu)

Technicians
Callie Eastburn (ce22@cornell.edu)
Debbie Ewing (dac42@cornell.edu)
Jim Ochsner (joo3@cornell.edu)
Michael M. Wheeler (mmw5@cornell.edu)

Undergraduates
Monica Bertoia (mlb55@cornell.edu)
Jim McNeil (jrm41@cornell.edu)
Andrea Savage (abs32@cornell.edu)

Publications (back to 1998)

Books

Hajek, A.E. 2004. Natural Enemies: An Introduction to Biological Control. Cambridge University Press.
http://us.cambridge.org/titles/catalogue.asp?isbn=0521653851

Hokkanen, H.M.T., and A.E. Hajek (editors). 2004. Environmental Impacts of Microbial Insecticides. Kluwer Academic Publishers, Dordrecht, NL.
http://www.wkap.nl/prod/b/1-4020-0813-9

Refereed publications (in reverse chronological order)

Dubois, T., A.E. Hajek, H. Jiafu & Z. Li. 2004. Evaluating the efficiency of entomopathogenic fungi against the Asian longhorned beetle, Anoplophora glabripennis (Coleoptera: Cerambycidae), by using cages in the field. Environ. Entomol. 33: 62-74.

Dubois, T., Z. Li, H. Jiafu & A.E. Hajek. 2004. Efficacy of fiber bands impregnated with Beauveria brongniartii cultures against the Asian longhorned beetle, Anoplophora glabripennis (Coleoptera: Cerambycidae). Biol. Contr. 31: 320-328.

Filotas, M.J. & A.E. Hajek. 2004. Influence of temperature and soil moisture on infection of forest tent caterpillars (Lepidoptera: Lasiocampidae) by the entomopathogenic fungus Furia gastropachae (Zygomycetes: Entomophthorales). Environ. Entomol. 33: 1127-1136.

Hajek, A.E., R.T. Curtiss & J.K. Liebherr. 2004. Characters differentiating male from female Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae). Proc. Entomol. Soc. Wash. 106: 928-931.

Hajek, A.E., N.W. Siegert, M.M. Wheeler & D. McCullough. 2004. Using bioassays to predict abundance of Entomophaga maimaiga resting spores in soil. J. Invertebr. Pathol. 86: 61-64.

Hajek, A.E., J.S. Strazanac, M.M. Wheeler, F. Vermeylen & L. Butler. 2004. Persistence of the fungal pathogen Entomophaga maimaiga and its impact on native Lymantriidae. Biol. Contr. 30: 466-471.

Delalibera Jr., I., A.E. Hajek & R.A. Humber. 2004. Neozygites tanajoae sp. nov., a pathogen of the cassava green mite. Mycologia 96: 1002-1009.

Delalibera Jr., I. & A.E. Hajek. 2004. Preservation of in vitro cultures of the mite pathogenic fungus Neozygites tanajoae. Can. J. Microbiol 50: 579-586.

Delalibera Jr., I. & A.E. Hajek. 2004. Pathogenicity and specificity of isolates of Neozygites tanajoae and Neozygites floridana (Zygomycetes: Entomophthorales) pathogenic to the cassava green mite. Biol. Contr. 30: 608-616.

Delalibera Jr., I., A.E. Hajek, and R.A. Humber. 2003. Use of cell culture media for cultivation of the mite pathogenic fungi Neozygites tanajoae and Neozygites floridana. J. Invertebr. Pathol. 84: 119-127.

Nielsen, C., A.E. Hajek, R.A. Humber, J. Bresciani, and J. Eilenberg. 2003. Soil as an environment for winter survival of aphid-pathogenic Entomophthorales. Biological Control 28: 92-100.

Hajek, A.E., A.B. Jensen, L. Thomsen, K.T. Hodge, and J. Eilenberg. 2003. Using PCR-RFLP to investigate relations among species in the entomopathogenic genera Eryniopsis and Entomophaga. Mycologia 95: 262-268.

Hajek, A.E., and C.C. Eastburn. 2003. Attachment and germination of Entomophaga maimaiga conidia on host and non-host larval cuticle. J. Invertebr. Pathol. 82: 12-22.

Filotas, M.J.F., A.E.Hajek, and R.A. Humber. 2003. Prevalence and biology of Furia gastropachae (Zygomycetes: Entomophthorales) in populations of the forest tent caterpillar (Lepidoptera: Lymantriidae). Can. Entomol. 135: 359-378.

Lopez Lastra, C.C., A.E. Hajek, and R.A. Humber. 2002. Comparing methods for preservation of cultures of entomopathogenic fungi. Can. J. Bot. 80: 1126-1130.

Hajek, A.E., M.J. Filotas, and D.C. Ewing. 2002. Formation of appressoria by two species of lepidopteran-pathogenic Entomophthorales. Can. J. Bot. 80: 220-225.

Hajek, A.E., C.C. Eastburn, C.I. Davis, and F. Vermeylen. 2002. Deposition and germination of conidia of the entomopathogen Entomophaga maimaiga infecting gypsy moth, Lymantria dispar. J. Invertebr. Pathol. 79: 37-43.

Lopez Lastra, C.C., D.M. Gibson, and A.E. Hajek. 2001. Survival and differential development of Entomophaga maimaiga and Entomophaga aulicae (Zygomycetes: Entomophthorales) in Lymantria dispar hemolymph. J. Invertebr. Pathol. 78: 201-209.

Klingen, I., A. Hajek, A. Renwick, and R. Meadow. 2002. Effect of brassicaceous plants on the survival and infectivity of insect pathogenic fungi. BioControl 47: 411-425.

Dubois, T., A.E. Hajek, and S. Smith. 2002. Methods for rearing the Asian longhorned beetle, Anoplophora glabripennis (Coleoptera: Cerambycidae) on artificial diet. Ann. Entomol. Soc. Amer. 95: 223-230.

Eilenberg, J., A. Hajek, and C. Lomer. 2001. Suggestions for unifying the terminology in biological control. BioControl 46: 387-400.

Hajek, A.E., and C.C. Eastburn. 2001. Effect of host insects on activation of Entomophaga maimaiga resting spores. J. Invertebr. Pathol. 77: 290-291.

Lopez Lastra, C.C., A.E. Hajek, and R.A. Humber. 2001. Effects of two cryopreservation techniques on viability and pathogenicity of entomophthoralean fungi. Can. J. Bot. 79: 861-864.

Jensen, M.A., J.E. Losey, and A.E. Hajek. 2001. Altered behavior and distribution of pea aphids, Acyrthosiphon pisum (Homoptera: Aphididae), infected with Pandora neoaphidis (Zygomycetes: Entomophthorales). BioControl 46: 337-343.

Hajek, A.E., M.M. Wheeler, C.C. Eastburn, and L.S. Bauer. 2001. Storage of resting spores of the gypsy moth fungal pathogen, Entomophaga maimaiga. Biocontrol Sci. Technol. 11: 637-647.

Hajek, A.E. 2001. Larval behavior in Lymantria dispar increases risk of fungal infection. Oecologia 126: 285-291.

Pilarska, D., M. McManus, A.E. Hajek, F. Hérard, F.E. Vega, P. Pilarska, and G. Markova. 2000. Introduction of the entomopathogenic fungus Entomophaga maimaiga Hum., Shim. & Sop. (Zygomycetes: Entomophthorales) to a Lymantria dispar (L.) (Lepidoptera: Lymantriidae) population in Bulgaria. Anz. Schadlingsk. 73: 125-126.

Hajek, A.E., L. Butler, J.K. Liebherr, and M.M. Wheeler. 2000. Risk of infection by the fungal pathogen Entomophaga maimaiga among Lepidoptera on the forest floor. Environ. Entomol. 29: 645-650.

Hajek, A.E., M. Shimazu, and B. Knoblauch. 2000. Isolating Entomophaga maimaiga using resting spore-bearing soil. J. Invertebr. Pathol. 75: 298-300.

Kogan, P.H., and A.E. Hajek. 2000. Formation of azygospores by the insect pathogenic fungus Entomophaga maimaiga in cell culture. J. Invertebr. Pathol. 75: 193-201.

Dahlsten, D.L., R.L. Zuparko, A.E. Hajek, D.L. Rowney, and S.H. Dreistadt. 1999. Long term sampling of Eucallipterus tiliae (Homoptera: Drepanosiphidiae) and associated natural enemies in a northern California site. Environ. Entomol.28: 845-850.

Hajek, A.E., C. Olsen, and J.S. Elkinton. 1999. Dynamics of airborne conidia of the gypsy moth (Lepidoptera: Lymantriidae) fungal pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales). Biol. Contr. 16: 111-117.

Hajek, A.E., and R.E. Webb. 1999. Inoculative augmentation of the fungal entomopathogen Entomophaga maimaiga as a homeowner tactic to control gypsy moth (Lepidoptera: Lymantriidae). Biol. Contr. 14: 11-18.

Malakar, R., J.S. Elkinton, A.E. Hajek, and J.P. Burand. 1999. Within-host interactions of Lymantria dispar L. (Lepidoptera: Lymantriidae) nucleopolyhedrosis virus (LdNPV) and Entomophaga maimaiga (Zygomycetes: Entomophthorales). J. Invertebr. Pathol. 73: 91-100.

Bidochka, M.J., and A.E. Hajek. 1998. A non-permissive entomophthoralean fungal infection increases activation of insect prophenoloxidase. J. Invertebr. Pathol. 72: 231-238.

Hajek, A.E., L. Bauer, M.L. McManus, and M.M. Wheeler. 1998. Distribution of resting spores of the Lymantria dispar pathogen Entomophaga maimaiga in soil and on bark. BioControl 43: 189-200.

Hajek, A.E., K.M. Tatman, P.H. Wanner, and M.M. Wheeler. 1998. Location and persistence of cadavers of gypsy moth, Lymantria dispar, containing Entomophaga maimaiga azygospores. Mycologia 90: 754-760.

Dwyer, G., J.S. Elkinton, and A.E. Hajek. 1998. Spatial scale and the spread of a fungal pathogen of gypsy moth. Amer. Nat. 152: 485-494.

Book Chapters

Hajek, A.E., I. Delalibera Jr., and L. Butler. 2003. Entomopathogenic fungi as classical biological control agents. In (H.M.T. Hokkanen & A.E. Hajek, Eds.) Environmental Impacts of Microbial Insecticides. Kluwer Academic Publishers, Dordrecht, NL.

Hajek, A.E. 2002. Biological control of insects and mites, pp. 57-60. In (D. Pimentel, Ed.) Encyclopedia of Pest Management. Marcel Dekker, NY [Invited review]

Hajek, A.E., S.P. Wraight, and J.D. Vandenberg. 2001. Control of arthropods using pathogenic fungi, pp. 309-347. In (S.B. Pointing & K.D. Hyde, Eds.) Bio-Exploitation of Fungi. Fungal Diversity Press, Hong Kong [Invited review.].

Pell, J., D. Steinkraus, J. Eilenberg, and A. Hajek. 2001. Exploring the potential of Entomophthorales in integrated crop management, pp. 71-167. In (T. Butt, C. Jackson, and N. Magan, Eds.) Fungal Biocontrol Agents: Progress, Problems and Potential. Kluwer, Dordrecht, Netherlands [Invited review.]

Goettel, M.S., A.E. Hajek, J.P. Siegel, and H.C. Evans. 2001. Safety of fungal biocontrol agents, pp. 347-375. In (T. Butt, C. Jackson, and N. Magan, Eds.) Fungal Biocontrol Agents: Progress, Problems and Potential. Kluwer, Dordrecht, Netherlands [Invited review.]

Goettel, M.S., and A.E. Hajek. 2001. Evaluation of non-target effects of pathogens used for management of arthropods, pp. 81-97. In (E. Wajnberg, J.K. Scott & P.C. Quimby, Eds.) Evaluating Indirect Ecological Effects of Biological Control. CABI Publ., Wallingford, Oxon, UK.

Hajek, A.E., and L. Butler. 2000. Predicting the host range of entomopathogenic fungi, pp. 263-276. In (P.A. Follett & J.J. Duan, Eds.) Non-target Effects of Biological Control. Kluwer, Dordrecht, Netherlands [Invited review.]

Hajek, A.E., I. Delalibera Jr., and M.L. McManus. 2000. Introduction of exotic pathogens and documentation of their establishment and impact, pp. 339-369. In (L.A. Lacey & H.K. Kaya, Eds.) Field Manual of Techniques in Invertebrate Pathology. Kluwer, Dordrecht, Netherlands [Invited review.].

Hajek, A.E., and M.S. Goettel. 2000. Guidelines for evaluating effects of entomopathogens on non-target organisms, pp. 847-868. In (L.A. Lacey & H.K. Kaya, Eds.) Field Manual of Techniques in Invertebrate Pathology. Kluwer, Dordrecht, Netherlands [Invited review.].

Hajek, A.E. 1999. Pathology and epizootiology of the lepidoptera-specific mycopathogen Entomophaga maimaiga. Microbiol. & Molecul. Biol. Rev. 63: 814-835 [Invited review.]

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