Source: UNIV OF MARYLAND submitted to NRP
DEVELOPING NEW APPROACHES FOR ECOLOGICALLY SUSTAINABLE MANAGEMENT OF PEST INSECTS
Sponsoring Institution
National Institute of Food and Agriculture
Project Status
COMPLETE
Funding Source
HATCH
Reporting Frequency
Annual
Accession No.
0219723
Grant No.
(N/A)
Cumulative Award Amt.
(N/A)
Proposal No.
(N/A)
Multistate No.
(N/A)
Project Start Date
Sep 1, 2009
Project End Date
Aug 31, 2012
Grant Year
(N/A)
Program Code
[(N/A)]- (N/A)
Recipient Organization
UNIV OF MARYLAND
(N/A)
COLLEGE PARK,MD 20742
Performing Department
Entomology
Non Technical Summary
Widespread concern about the hazards of synthetic insecticides, coupled with widespread evolution of pest resistance to those compounds, have made the development of alternative measures for the management of insect pests an urgent task for entomologists. The common goal that binds together the projects in this proposal is the search for novel approaches to pest management that avoid can hazards of both kinds. The diversity of these sub-projects reflects the necessity to explore as many aspects of insect biology as possible, in order to find new ways of suppressing pest populations. The specific studies to be conducted are as follows. (1) We will test the three main hypotheses that have been advanced to explain the fact that trees in landscape plantings which have been treated with the systemic insecticide imidacloprid are often subject to devastating outbreaks of spider mites. Discovery of the underlying mechanism should help identify ways to avert these mite outbreaks, and help us better understand and control pest outbreaks in general. (2) We will conduct a genomic analysis of geographic variation in the progress toward specialization and speciation on different hosts of an introduced pest of forage crops, the pea aphid (Acyrthosiphon pisum,Homoptera: Aphididae). Understanding the ecological and genetic mechanisms of specialization can help to discover management tactics that can derail the evolutionary processes that lead to host plant specialization in pest species. (3)We will investigate the viability and efficacy of entomopathogenic (insect-attacking) nematode worms as a sustainable non-chemical means of controlling root-feeding pests of field and turf crops in Maryland. (4) We will test new approaches for preventing contamination of the environment by entomopathogenic (insect-attacking) fungi (EPFs) which have been genetically engineered for increased ability to kill pest insects, thereby alleviating biosafety obstacles to widespread application of this promising new pest management technology. We engineered the gene for an insect toxin from a scorpion into the fungus, in such a way as to have the toxin produced only when the fungal cells are inside the pest insect. This prevents the toxin from contaminating the environment. We now need to develop technology that can block both spread of the engineered fungus in the environment, and its possibility for interbreeding with wild counterparts. (5) We will investigate an apparent case of genetic differentiation and speciation in progress in a native holly leaf miner fly (Phytomyza glabricola; Diptera: Agromyzidae), driven by the recent separation of its host plant into two species. An understanding of the process of population divergence and speciation is central to understanding how agricultural and horticultural insect communities have evolved, and hence how they are likely to change under selection imposed by pest management practice. We will use both genetic analysis and cross-mating and cross-rearing experiments to determine the the degree and kind of differentiation that has thus far developed between the two putative ?host races? of the holly leafminer and their host plants.
Animal Health Component
(N/A)
Research Effort Categories
Basic
(N/A)
Applied
(N/A)
Developmental
(N/A)
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2112110113020%
2113110108040%
2153130107020%
2154020108020%
Knowledge Area
211 - Insects, Mites, and Other Arthropods Affecting Plants; 215 - Biological Control of Pests Affecting Plants;

Subject Of Investigation
2110 - Ornamental trees and shrubs; 3130 - Nematodes; 4020 - Fungi; 3110 - Insects;

Field Of Science
1130 - Entomology and acarology; 1070 - Ecology; 1080 - Genetics;
Goals / Objectives
Develop scientific basis for new methods of controlling pest insects without using synthetic chemical pesticides, by clarifying and exploiting diverse aspects of the biology of insects and their natural enemies, including: (1)the mechanisms underlying outbreaks of spider mites on trees which have been treated with the insecticide imidacloprid; (2) the degree to which populations of the pea aphid associated with clover versus alfalfa constitute genetically isolated host races, in the eastern versus the western U.S.; (3)the viability and efficacy of entomopathogenic nematode worms as inoculative control agents for root-feeding pests of field and turf crops; (4)mechanisms that slow the spread of, and gene flow from, transgenically hypervirulent insecticidal organisms;(5)Host-associated divergence and phylogeography of host races of the holly leafminer.
Project Methods
1) Standard field, laboratory and statistical methods will be used to determine whether, on foliage of three test plant species, imidacloprid treatment either reduces survival of spider mite predators or increases lifespan or fecundity of spider mites. (2) To determine the degree and kind of genetic isolation between pea aphid populations we will sample populations on multiple hosts at multiple localities for multi-locus genotype frequencies, using DNA markers with known positions on a genetic linkage map. That map, based on both 93 AFLP markers and 150 microsatellite markers, includes previously-identified chromosomal blocks (QTL) that influence key phenotypic traits involved in divergence and speciation. (3) To determine the distribution and potential biocontrol utility of entomopathogenic nematodes in Maryland, we will extract soil cores at multiple localities, and test for nematodes using a highly susceptible lab-reared host, caterpillar of the greater wax moth (Galleria mellonella), as bait. Using standard laboratory protocols, with Galleria as a control, we will then test the ability of the nematodes found to kill potential host species found in the same habitats. (4)We will use a two-step procedure to testing possible mechanisms for mitigating the spread of and gene flow from transgenically hypervirulent strains of Metarhizium fungus. First, we will try insert into these strains genes which should mitigate transmission because, in the anti-sense form, they suppress sporulation or other traits essential to spread of the fungus. We will test numerous candidate genes which are already known to control different stages of spore formation. Having selected appropriate candidates, we will then create hypervirulent strains in which the hypervirulence gene is adjacent to the the transmission-mitigating genes. This should have the effect that any recombinants with the native strains of the fungus should have very low fitness, further lowering the chance of unintentional spread of the virulence gene. (5) We will use both genetic analysis and cross-mating and cross-rearing experiments to ascertain the degree and kind of differentiation exhibited by the two putative host races of the holly leafminer and their host plants. We will test the ability of larvae from each host race to survive on the host plant of the other, and we will test for assortative mating among adults of the two putative races. For genetic analyses, we will sample 30-100 individual insects from each host plant species at each location, along with their host individuals. DNA will be extracted from insects and plants and mtDNA fragments will be sequenced from the insects, using COI primers already found to be both robust and variable. We will also develop methods for analysis of similarly behaving DNA markers from the plants. In addition, we will generate several hundred AFLP markers for both insects and host plants.

Progress 09/01/09 to 08/31/12

Outputs
Target Audience: results of our research findings have been disseminated to more than 12,000 green industry members and volunteers that work and live in urban forests at local, regional, national, and international meeting via more than 100 professional meetings, workshops, shortcourses, and/or conferences. During the reporting period, we have provided information to scientists, businesses, agencies, and the general public on the ecology and management of pests in urban forests to more than 20 million people through professional and lay publications and on international, national, and local television, print, radio, and web-based media venues. Changes/Problems: Nothing Reported What opportunities for training and professional development has the project provided? We provided training for 2 high school students, 29 undergraduate students, 12 graduate students, and four postdocs. How have the results been disseminated to communities of interest? In addition to our scholarly publications, results of our research findings have been disseminated to more than 12,000 green industry members and volunteers that work and live in urban forests at local, regional, national, and international meeting via more than 100 professional meetings, workshops, shortcourses, and/or conferences. During the reporting period, we have provided information to scientists, businesses, agencies, and the general public on the ecology and management of pests in urban forests to more than 20 million people through professional and lay publications and on international, national, and local television, print, radio, and web-based media venues. Our publications are read and cited. Our research findings are sought after for conference, meetings, and symposia. Our trainings receive excellent ratings for content. What do you plan to do during the next reporting period to accomplish the goals? Nothing Reported

Impacts
What was accomplished under these goals? Our comprehensive reviews of arthropods along urban gradients reveal that many herbivorous taxa from several feeding guilds with diverse life histories, modes of dispersal, and host specificities outbreak along urban gradients. Small sucking arthropods like scale insects and mites dominate eruptive taxa in cities. These multivoltine pests with short generation times may be advantaged by elevated temperatures in cities. Strong theoretical evidence and several empirical studies indicate that many taxa benefit from enhanced resource quality linked to greater quantity or availability of nutrients and impaired plant defenses wrought by periods of intermittent drought and pulsed inputs of water, nutrients, and pollutants. Relaxation of top-down suppression associated with reduced richness or abundance of natural enemies are implicated in outbreaks of herbivores in cities which may lack of critical resources such as abundant alternative prey for generalists. Physical structures in cities provide spatial refuge for pests from natural enemies and elevated temperatures may provide temporal escape from predators and parasitoids and unfavorable thermal regimes. Natural enemies are important regulators of forest pests and pesticides often remove natural enemies, impair their activities, alter plant quality, or stimulate reproduction in pests thereby contributing to outbreaks in urban areas. Invasive species such as sap-sucking sternorryncha pass through genetic bottlenecks that can reduce genetic variation and phenotypic traits such as dietary breadth. Pesticides are important management tools for invasive pests in urban forests, but their use in eradication programs may result in secondary pest outbreaks. We found that neonicotinoid insecticides suppress defensive pathways in plants and kill natural enemies that consume insecticide tainted prey. We provided a model for developing management programs for Emerald Ash Borer, Agrilus planipennis, based on rate of spread, cost of management, and benefit of the protected resource, namely urban ash trees. We discovered a new mode of feeding in Brown Marmorated Stink Bug, Halyomorpha halys, and identified patterns of host use. This information will allow us to design residential and commercial landscapes refractory to this pest by plant selection. Our syntheses inform urban planners and resource managers about taxa of arthropods most likely to outbreak along urban gradients and identify key mechanisms that underlie these outbreaks. Due to the anthropogenic etiology of many of these mechanisms, landscape managers can develop management approaches that rely on elements of design, plant culture, and biological control to suppress pest outbreaks. This will ultimately result in reduced economic and environmental costs of managing pests while enhancing the sustainability of urban forests. We have genotyped several hundred pea aphids from alfalfa and red clover in both New York and WA state for 174 microsatellite loci and 945 SNP markers. We have localized genomic regions affecting host plant specialization in the New York populations using a linkage map and QTL analysis. These results show that genomic regions on all 4 chromosomes affect host plant specialization, making host plant specialization in this species a highly polygenic trait. We have also found that pea aphid populations on red clover in WA are genetically differentiated from clover populations in New York. Our data suggest that the pea aphid populations on red clover in WA are more likely to have evolved from local populations inhabiting alfalfa than from eastern red clover populations, suggesting an independent evolution of specialization in western pea aphids. Experimental tillage treatment in soy and corn field crops in 2009-2011 at five MAES facilities (Beltsville, Keedysville, Salisbury, Upper Marlboro, Wye) demonstrated that entomopathogenic nematodes were sensitive to conventional tillage relative to conservation till. Species richness and relative abundance of these beneficial nematodes were approximately halved under conventional till. Nematodes applied as control agents for the small hive beetle (Aethina tumida) were effective in lab but not in field trials in 2010 and 2011.

Publications

  • Type: Journal Articles Status: Awaiting Publication Year Published: 2014 Citation: Heffernan, J.B., P.A. Soranno, M.J. Angilletta, Jr, L.B. Buckley, D.S. Gruner, T.H. Keitt, J.R. Kellner, J.S. Kominoski, A.V. Rocha, J. Xiao, T.K. Harms, S.J. Goring, L.E. Koenig, W.H. McDowell, H. Powell, A.D. Richardson, C.A. Stow, R. Vargas, and K.C. Weathers. 2014 (in press). Macrosystems ecology: understanding ecological pattern and process at continental scales. Frontiers in Ecology and the Environment
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Kawahara A.Y., Ohshima I., Kawakita A., Regier J.C., Mitter C., Cummings M.P., Davis D.R.,Wagner D.L., De Prins J., Lopez-Vaamonde C. 2011. Increased gene sampling provides stronger support for higher-level groups within gracillariid leaf mining moths and relatives (Lepidoptera: Gracillariidae). BMC Evolutionary Biology 11:182.
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Zwick, A., J. C. Regier, C. Mitter, M. P. Cummings. 2011. Increased gene sampling yields robust support for higher-level clades within Bombycoidea (Lepidoptera). Systematic Entomology 36: 3143.
  • Type: Journal Articles Status: Published Year Published: 2014 Citation: Cavanaugh, K.C., J.R. Kellner, A.J. Forde, D.S. Gruner, J.D. Parker, W. Rodriguez, and I.C. Feller. 2014. Poleward expansion of mangroves is a threshold response to decreased frequency of extreme cold events. Proceedings of the National Academy of Sciences 111:723-727
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Lind, E., E.T. Borer, E. Seabloom, P.B. Adler, J.D. Bakker, D. Blumenthal, M.J. Crawley, K. Davies, J. Firn, D.S. Gruner, W.S. Harpole, Y. Hautier, H. Hillebrand, J.M.H. Knops, B.A. Melbourne, B. Mortensen, A.C. Risch, M. Schuetz, C. Stevens, and P.D. Wragg. 2013. Life history constraints in grassland plant species: a growth-defense tradeoff is the norm. Ecology Letters 16:513-521
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Borer, E.T., M.E.S. Bracken, E.W. Seabloom, J.E. Smith, J. Cebrian, E.E. Cleland, J.J. Elser, W.F. Fagan, D.S. Gruner, W.S. Harpole, H. Hillebrand, A.J. Kerkhoff, and J.T. Ngai. Global biogeography of autotroph chemistry: is insolation a driving force? Oikos 122:1121-1130
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Gruner, D.S. 2013. Trophic Cascades. Encyclopedia of Life Sciences (eLS), John Wiley & Sons, Ltd., Chichester. doi:10.1002/9780470015902.a0003183.pub2
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Thompson, B.M., R.J. Grebenok, S.T. Behmer, and D.S. Gruner. 2013. Microbial symbionts shape the sterol profile of the xylem-feeding woodwasp, Sirex noctilio. Journal of Chemical Ecology 38:129-139
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Gruner, D.S. and K.A. Mooney. 2013. Green grass and high tides: grazing lawns in terrestrial and aquatic ecosystems. Oikos 122:313316
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Herlihy, M.V., R.G. Van Driesche, M.R. Abney, J. Brodeur, A.B. Bryant, R.A. Casagrande, D.A. Delaney, T.E. Elkner, S.J. Fleischer, R.L. Groves, D.S. Gruner, J.P. Harmon, G.E. Heimpel, K. Hamady, T.P. Kuhar, C.M. Maund, A.M. Shelton, A.J. Seaman, M. Skinner, R. Weinzierl, K.V. Yeargan, and Z. Zendrei. 2012. Distribution of Cotesia rubecula (Hymenoptera: Braconidae) and its displacement of Cotesia glomerata in eastern North America. Florida Entomologist 95:458-464
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Adler, P.B., E.W. Seabloom, E.T. Borer, H. Hillebrand, Y. Hautier, A. Hector, W.S. Harpole, L.R. OHalloran, J.B. Grace, T.M. Anderson, J.D. Bakker, L.A. Biederman, C.S. Brown, Y.M. Buckley, L.B. Calabrese, C.-J. Chu, E.E. Cleland, S.L. Collins, K.L. Cottingham, M.J. Crawley, E.I. Damschen, K.F. Davies, N.M. DeCrappeo, P.A. Fay, J. Firn, P. Frater, E.I. Gasarch, D.S. Gruner, N. Hagenah, J. HilleRisLambers, H. Humphries, V.L. Jin, A.D. Kay, K.P. Kirkman, J.A. Klein, J.M.H. Knops, K.J. La Pierre, J.G. Lambrinos, W. Li, A.S. MacDougall, R.L. McCulley, B.A. Melbourne, C.E. Mitchell, J.L. Moore, J.W. Morgan, B. Mortensen, J.L. Orrock, S.M. Prober, D.A. Pyke, A.C. Risch, M. Schuetz, M.D. Smith, C.J. Stevens, L.L. Sullivan, G. Wang, P.D. Wragg, J.P. Wright, and L.H. Yang. 2011. Productivity is a poor predictor of plant species richness. Science 333:1750-1753
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Harpole, W.S., J.T. Ngai, E.E. Cleland, E.W. Seabloom, E.T. Borer, M.E.S. Bracken, J.J. Elser, D.S. Gruner, H. Hillebrand, J.B. Shurin, and J.E. Smith. 2011. Nutrient co-limitation of plant communities. Ecology Letters 14:852-862
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Pearson, R.E.G., S.T. Behmer, D.S. Gruner, and R.F. Denno. 2011. Effects of diet quality on performance and nutrient regulation in an omnivorous katydid. Ecological Entomology 36:471-479
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Fang W, Vega-Rodriguez, J., Ghosh, A.K., Jacobs-Lorena, M., Khang, A and St. Leger, R.J., 2011. Development of transgenic fungi that kill human malaria parasites in mosquitoes Science 331: 1074-1077.
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Gao Q, Jin K, Ying S-H, Zhang Y, Xiao G, et al. (2011) Genome Sequencing and Comparative Transcriptomics of the Model Entomopathogenic Fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7(1): e1001264. doi:10.1371/journal.pgen.1001264
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Pava-Ripoll, M., Angelini, C, Fang W., Wang, S, Posada F, St. Leger, R. 2011 The rhizosphere competent entomopathogen Metarhizium anisopliae expresses a specific subset of genes in plant root exudates. Microbiology 157: 47-55
  • Type: Journal Articles Status: Published Year Published: 2010 Citation: Fang W, Fernandes EK, Roberts DW, Bidochka MJ, St Leger RJ. 2010 A laccase exclusively expressed by Metarhizium anisopliae during isotropic growth is involved in pigmentation, tolerance to abiotic stresses and virulence. Fungal Genet Biol; 47:602-7
  • Type: Journal Articles Status: Published Year Published: 2010 Citation: Fang, W and St. Leger, R.J., 2010 Mrt, a gene unique to fungi, encodes an oligosaccharide transporter and facilitates rhizosphere competency in Metarhizium robertsii Plant Physiol. 154: 1549-1557
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Fang W, St. Leger RJ (2012) Enhanced UV Resistance and Improved Killing of Malaria Mosquitoes by Photolyase Transgenic Entomopathogenic Fungi. PLoS ONE 7(8): e43069. doi:10.1371/journal.pone.0043069
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Xiao G, Ying SH, Zheng P, Wang ZL, Zhang S, Xie XQ, Shang Y, St Leger RJ, Zhao GP, Wang C, Feng MG. 2012. Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci. Rep. 2, 483; DOI:10.1038/srep00483
  • Type: Book Chapters Status: Published Year Published: 2013 Citation: Wang, C and St. Leger, R.J. 2013. Genomics of Entomopathogenic Fungi. In Ecological Genomics of the Fungi (ed. Francis Martin)
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Via, S. 2012. Divergence hitchhiking and the dynamics of ecological speciation-with-gene-flow. Phil. Trans. R. Soc. B 2012 367, 451-460. doi: 10.1098/rstb.2011.0260
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Via S, Conte G, Mason?Foley C, Mills K. 2012. Localizing FST outliers on a QTL map reveals evidence for large genomic regions of reduced gene exchange during speciation?with?gene?flow. Molecular Ecology, 21, 5546-5560.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: J Ferrari, JA West, S Via, HCJ Godfray. 2012. Population genetic structure and secondary symbionts in host?associated populations of the pea aphid complex. Evolution 66, 375-390.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2011 Citation: Hawthorne DJ, Dively GP (2011) Killing Them with Kindness? In-Hive Medications May Inhibit Xenobiotic Efflux Transporters and Endanger Honey Bees. PLoS ONE 6(11): e26796. doi: 10.1371/journal.pone.0026796
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Alexander, L. C., Hawthorne, D. J., Palmer, M. A. and W.O. Lamp. 2011. Loss of genetic diversity in the North American mayfly Ephemerella invaria associated with deforestation of headwater streams. Freshwater Biology.
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Mitter KT, Larsen TB, de Prins W, De Prins J, Collins S, Hawthorne, DJ, et al. 2011 The butterfly subfamily Pseudopontiinae is not monobasic: marked genetic diversity and morphology reveal three new species of Pseudopontia (Lepidoptera: Pieridae). Systematic Entomology 36: 139-163.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Frank D. Rinkevich, Cathy Su, Tom�s A. Lazo, David J. Hawthorne, Ward M. Tingey, Samir Naimov, Jeffrey G. Scott. 2012. Multiple evolutionary origins of knockdown resistance (kdr) in pyrethroid-resistant Colorado potato beetle, Leptinotarsa decemlineata. Pesticide Biochemistry and Physiology 104: 192-200
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Hebert JB, Scheffer SJ, Hawthorne DJ (2013) Reproductive Isolation between Host Races of Phytomyza glabricola on Ilex coriacea and I. glabra. PLoS ONE 8(9): e73976. doi: 10.1371/journal.pone.0073976
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Liao X, Fang, W and St. Leger, R.J. 2013. Overexpression of a Metarhizium robertsii HSP25 gene increases thermotolerance and survival in soil. Applied Microbiology and Biotechnology DOI 10.1007/s00253-013-5360-5
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Liao X, Fang W, Lin L, Lu H-L, St. Leger RJ (2013) Metarhizium robertsii Produces an Extracellular Invertase (MrINV) That Plays a Pivotal Role in Rhizospheric Interactions and Root Colonization. PLoS ONE 8(10): e78118. doi:10.1371/journal.pone.0078118
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Wang, S., Fang, W., Wang, C. and St. Leger, R.J. 2011. Insertion of an esterase gene into a specific locust pathogen (Metarhizium acridum) enables it to infect caterpillars. PLoS Pathog 7(6): e1002097. doi:10.1371/journal.ppat.1002097
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Wang, S. OBrien, T., Pava-Ripoll, M and St. Leger, R.J. 2011 Local adaptation of an introduced transgenic insect fungal pathogen due to new beneficial mutations. Proc. Natl. Acad. Sci. USA 108: 20449-20454.
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Lin, L., Fang, W. Liao, X., Wang, F., and St. Leger RJ 2011 The MrCYP52 cytochrome P450 monoxygenase gene of Metarhizium robertsii is important for utilizing insect epicuticular hydrocarbons. PLoS ONE 6(12): e28984. doi:10.1371/journal.pone.0028984
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Sargent, C., H. M. Martinson, and M. J. Raupp. 2011. The Orient express in Maryland: The Brown Marmorated Stink bug, Halymorpha halys (St�l) (Hemiptera: Pentotomidae). The Maryland Entomologist. 5 (3):221.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Leskey, T. C., G. C. Hamilton, A. L. Nielsen, D. Polk, C. Rodriguez-Saona, J. C. Bergh, A. Herbert, T. Kuhar, D., Pfeiffer, G. Dively, C. Hooks, M. Raupp, P. Shrewsbury, G. Krawczyk, P.W. Shearer, J. Whalen, C. Koplinka-Loehr, E. Myers, D. Inkley, K. Hoelmer, D. Lee, and S. E. Wright. 2012. Pest Status of the Brown Marmorated Stink Bug, Halyomorpha halys (St�l) in the USA. Outlooks in Pest Management. 23:218-236.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Szczepaniec, A., and M.J. Raupp. 2012. Direct and indirect effects of imidacloprid on fecundity and abundance of Eurytetranychus buxi (Acari: Tetranychidae) on boxwoods. Exp. Appl. Acarol. DOI 10.1007/s10493-012-9614-1.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Szczepaniec, A., and M.J. Raupp. 2012. Effects of imidacloprid on boxwood spider mite (Acari: Tetranychidae) abundance and associated injury to boxwoods. Journal of Arboriculture and Urban Forestry. 38(2): 37-39.
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Eubanks, M.D., M.J. Raupp, D.L. Finke 2011. D. Robert F. Denno (1945 2008): Insect Ecologist Extraordinaire. Annual Review of Entomology. 56:273-292.
  • Type: Journal Articles Status: Published Year Published: 2010 Citation: Sargent, C., M. J. Raupp, D. Bean, and A. J. Sawyer. 2010. Dispersal of Emerald Ash Borer within an Intensively Managed Quarantine Zone. Journal of Arboriculture and Urban Forestry. 36: 160-163.
  • Type: Books Status: Published Year Published: 2011 Citation: Raupp, M.J. 2011. Twenty six things that bug me. Barclay Bryan. Port Republic, MD. 30 pp.
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Szczepaniec, A. , S. F. Creary, K. L. Laskowski, J.P. Nyrop and M. J. Raupp. 2011. Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes. PLoS ONE 6(5): e20018. doi:10.1371/journal.pone.0020018PloS. ONE.
  • Type: Journal Articles Status: Published Year Published: 2010 Citation: Raupp, M.J., P.M. Shrewsbury, and D.H. Herms. 2010. Ecology of herbivorous arthropods in urban landscapes. Annual Review of Entomology. 55:19-38.
  • Type: Books Status: Published Year Published: 2010 Citation: Davidson, J. A. and M. J. Raupp. 2010. Second edition. Managing insects and mites on woody plants: An IPM approach. Tree Care Industry. Londonderry, NH. 177 pp.
  • Type: Book Chapters Status: Awaiting Publication Year Published: 2014 Citation: Raupp, M.J., Shrewsbury, P.M. and D. H. Herms. In press. Disasters by design: Outbreaks along urban gradients. In: Insect outbreaks revisited. P. Barbosa, D. Letourneau, and A. Agrawal eds. Wiley-Blackwell, Oxford, UK.
  • Type: Conference Papers and Presentations Status: Awaiting Publication Year Published: 2014 Citation: Martinson, H., C. Sargent, D. Bean, A. Sawyer, and M. Michael Raupp. In press. Predicting movement risk, and economic impact of emerald ash borer in Maryland. Proceedings of the 21st USDA Interagency research forum on invasive species. Annapolis, MD.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Sohn, J-C, J.C. Regier, C. Mitter, D. R. Davis, J.F. Landry, A. Zwick and M. P. Cummings. 2013. A molecular phylogeny for Yponomeutoidea (Insecta, Lepidoptera, Ditrysia) and its implications for classification, biogeography and the evolution of host plant use. PLoS One 8(1): e55066. doi:10.1371/journal.pone.0055066.
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Bazinet, A.L., M.P. Cummings, K.T.Mitter and C. Mitter. 2013. Can RNA-Seq resolve the rapid radiation of advanced moths and butterflies (Lepidoptera: Apoditrysia)? An exploratory study. PLoS ONE 8 (12): e82615. doi:10.1371/journal.pone.0082615
  • Type: Journal Articles Status: Published Year Published: 2013 Citation: Regier, J.C., C. Mitter, A. Zwick, A. L. Bazinet, M. P. Cummings, A.Y. Kawahara, J.-C. Sohn, D. J. Zwickl, S. Cho, D. R. Davis, J. Baixeras, J.W. Brown, C. Parr, S.J. Weller, D.C. Lees, K. T. Mitter. 2013. A large-scale, higher-level, molecular phylogenetic study of the insect order Lepidoptera (moths and butterflies). PLoS ONE 8(3): e58568. doi:10.1371/ journal.pone.0058568
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Regier, J., C. Mitter, M.A. Solis, J.E. Hayden, B. Landry, M. Nuss, T. Simonsen, S.-H. Yen, A. Zwick, M. P. Cummings. 2012. A molecular phylogeny for the pyraloid moths (Lepidoptera: Pyraloidea) and its implications for higher-level classification. Systematic Entomology 37: 635-656.
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Sohn, J., C. Labandeira, D.R. Davis & C. Mitter. 2012. An annotated catalog of fossil and subfossil Lepidoptera (Insecta: Holometabola) of the world. Zootaxa 3286: 1132
  • Type: Journal Articles Status: Published Year Published: 2012 Citation: Regier, J.C., J.W. Brown, C. Mitter, J. Baixeras, S. Cho, M. P. Cummings, & A. Zwick. 2012. A molecular phylogeny for the leaf-roller moths (Lepidoptera: Tortricidae) and its implications for classification and life history evolution. PLoS One 7: e35574. doi:10.1371/journal.pone.0035574
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: van Nieukerken, E. J., Kaila, L., Kitching, I. J., Kristensen, N. P., Lees, D. C., Minet, J., Mitter, C., Mutanen, M., Regier, J. C., Simonsen, T. J., Wahlberg, N., Yen, S.-H., Zahiri, R., Adamski, D., Baixeras, J., Bartsch, D., Bengtsson, B. �., Brown, J. W., Bucheli, S. R., Davis, D. R., De Prins, J., De Prins, W., Epstein, M. E., Gentili-Poole, P., Gielis, C., H�ttenschwiler, P., Hausmann, A., Holloway, J. D., Kallies, A., Karsholt, O., Kawahara, A., Koster, S. J. C., Kozlov, M., Lafontaine, J. D., Lamas, G., Landry, J.-F., Lee, S., Nuss, M., Penz, C., Rota, J., Schmidt, B. C., Schintlmeister, A., Sohn, J. C., Solis, M. A., Tarmann, G. M., Warren, A. D., Weller, S., Yakovlev, R., Zolotuhin, V. & Zwick, A. 2011. Order Lepidoptera Linnaeus, 1758. In: Zhang, Z.-Q. (Ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148: 212221.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2014 Citation: Hautier, Y., E. Seabloom, E.T. Borer, P. Adler, W.S. Harpole, H. Hillebrand, E. Lind, A. MacDougall, C. Stevens, J.D. Bakker, Y. Buckley, C. Chu, S.L. Collins, P. Daleo, E.I. Damschen, K. Davies, P.A. Fay, J. Firn, D.S. Gruner, V.L. Jin, J.A. Klein, J.M. H. Knops, K.J. La Pierre, W. Li, R. McCulley, B. Melbourne, J.L. Moore, L.R. O�"Halloran, S.M. Prober, A.C. Risch, M. Sankaran, M. Schuetz, and A. Hector. 2014 (in press). Eutrophication weakens stabilizing effects of diversity in natural grasslands. Nature doi:10.1038/nature13014
  • Type: Journal Articles Status: Published Year Published: 2011 Citation: Cho, S., A. Zwick, J. C. Regier, C. Mitter, M. P. Cummings, J. Yao, Z. Du, H. Zhao, A.Y. Kawahara, S. Weller, D. R. Davis, J. Baixeras, J.W. Brown, C. Parr. 2011. Can Deliberately Incomplete Gene Sample Augmentation Improve a Phylogeny Estimate for the Advanced Moths and Butterflies (Hexapoda: Lepidoptera)? Systematic Biology 60: 782796.
  • Type: Journal Articles Status: Awaiting Publication Year Published: 2014 Citation: Thompson, B.M., J. Bodart, C. McEwen, and D.S. Gruner. 2014 (in press). Adaptations for symbiont-mediated external digestion in Sirex noctilio Fab. (Hymenoptera: Siricidae). Annals of the Entomological Society of America