Silverman, Jules

Charles G. Wright Distinguished Professor

Program area: 

Urban Entomology, Insect Behavior, Nutritional Ecology

Office: 

3314 Gardner Hall

NCSU - Campus Box 7613
Raleigh, NC USA  27695-7613

Phone: 
919.513.2468
Fax: 
919.515.7746
Education: 
  • B.S State University of New York at Fredonia (1975)
  • M.S. University of California at Riverside (1978)
  • Ph.D. University of California at Riverside (1981)
Research: 

Behavioral resistance and bait aversion in Blattella germanica

The German cockroach, Blattella germanica, is a significant pest within human-built structures and continues to be an important target of the pest control industry.  Currently, chemical insecticides are utilized in attempts to control German cockroaches, with baits being the favored product form for the past 30 years. Nearly 20 years ago the industry was alerted to failures in cockroach control with baits due to an unusual form of resistance now widely recognized as bait aversion (behavioral resistance).  Bait aversion develops when initially a very small fraction of B. germanica within a population reject a component of the bait matrix. Over time, as non-bait averse individuals are eliminated, bait-averse individuals proliferate and represent most of the population. What was surprising in this case was that cockroaches no longer consumed bait because of an aversion to an ingredient used to stimulate cockroaches to feed, glucose (pdf). Thus, cockroaches that favored glucose were killed by consuming the toxic matrix while glucose-avoiders survived producing subsequent generations of bait/glucose avoiders.  Although avoiding glucose is costly in normal foraging activities on insecticide-free foods (pdf), this trait confers greater survivorship under the strong selection pressure of toxic baits. We recently determined that glucose-averse behavior could be elicited through sensilla on the antennae and mouthparts (pdf) and that changes in peripheral gustatory coding underlie this novel trait. Whereas glucose elicits strong neuronal responses from the sugar gustatory receptor neurons (GRNs) of wild-type cockroaches, in glucose-averse cockroaches it elicits responses from both the sugar and deterrent (bitter) GRNs (pdf).

My efforts to understand this phenomenon span several levels of biological organization and include projects in collaboration with Dr. Coby Schal.

Ant behavioral and community ecology and the management of urban pest ants

The Argentine ant, Linepithema humile, is a particularly troublesome invasive species.  Argentine ant populations have disrupted native ant and other arthropod communities and their negative impact is evident across different trophic levels through the elimination of rare pollinators and predators.  Because Argentine ants consume honeydew produced by hemipterans, they are considered serious agricultural pests, particularly of citrus, as they tend crop feeding hemipteran species and interfere with their natural enemies. Thus, I am particularly interested in how Argentine ants, vs. native ants; facilitate hemipteran populations and how hemipterans fuel Argentine ant colony growth.

The Asian needle ant, Pachycondyla chinensis, is a relatively new invader to forest and urban habitats in the easterns US. Interestingly, it has displaced the Argentine ant in certain habitats. We are tracking population-level interactions between these two invasive ants and elucidating the behavioral mechanism(s) underlying this displacement process.

Teaching: 

ENT 509 Biology of Aquatic Insects
ENT 601/801 Seminar - Insect Mutualisms

Publications

 

  1. Shik J.Z., C. Schal and J. Silverman.  2014.  Diet specialization in an extreme omnivore: nutritional regulation in glucose-averse German cockroaches.  Journal of Evolutionary Biology. 27:2096-2105.(PDF)
  2. Shik J.Z., A.D. Kay and J. Silverman. 2014. Aphid honeydew provides a nutritionally balanced resource for incipient Argentine ant mutualists. Animal Behaviour. 95:33–39 (PDF)
  3. Bednar D.M., J.Z. Shik and J. Silverman 2013. Prey handling performance facilitates competitive dominance of an invasive over native keystone ant. Behavioral Ecology. 24: 1312-1319 (PDF)
  4. Spicer-Rice E. and J. Silverman 2013. Submissive behaviour and habituation facilitate entry into habitat occupied by an invasive ant. Animal Behaviour. 86: 497-506. (PDF) Editor's feature (PDF)
  5.  Wada-Katsumata A., J. Silverman and C. Schal. 2013. Changes in taste neurons support the emergence of an adaptive behavior in cockroaches. Science. 340: 972-975. (PDF)
  6.  Spicer-Rice E. and J. Silverman 2013. Propagule pressure and climate contribute to the displacement of Linepithema humile by Pachycondyla chinensis. PLoS ONE 10.1371/journal.pone.0056281. (PDF)
  7. Shik J.Z. and J. Silverman. 2013. Towards a nutritional ecology of invasive establishment: aphid mutualists provide better fuel for incipient Argentine ant colonies than insect prey. Biological Invasions 15:829-836. (PDF)
  8. Spicer-Rice E., J.Z. Shik and J. Silverman. 2012. Effect of scattered and discrete hydramethylnon bait placement on the Asian needle ant, Pachycondyla chinensis Emery. Journal of Economic Entomology 105:1751-1757. (PDF)
  9. Vasquez G.M., E. L. Vargo and J. Silverman 2012. Fusion between southeastern US Argentine ant colonies and its effect on colony size and productivity. Annals of the Entomological Society of America 105: 268-274. (PDF)
  10. Guenard B and J. Silverman. 2011. Tandem carrying, a new foraging strategy in ants: description, function and adaptive significance relative to other described foraging strategies. Naturwissenschaften 98: 651-659.(PDF)
  11. Wada-Katsumata A., J. Silverman and C. Schal. 2011. Differential inputs from chemosensory appendages mediate feeding responses to glucose in wild-type and glucose-averse German cockroaches, Blattella germanica. Chemical Senses 36: 589–600.(PDF)
  12. Brightwell R.J. and J. Silverman. 2011. The Argentine ant persists through unfavorable winters via a mutualism facilitated by a native tree. Environmental Entomology 40: 1019-1026.(PDF)
  13. Bednar DM and J. Silverman. 2011. Use of termites, Reticulitermes virginicus, as a springboard in the invasive success of a predatory ant, Pachycondyla (=Brachyponera) chinensis. Insectes Sociaux 58: 459-467. (PDF)
  14. Menke S. B., B. Guénard,  J. O. Sexton, M. D. Weiser,  R. Dunn and J. Silverman. 2011 Urban areas may serve as habitat and corridors for dry-adapted, heat tolerant species; an example from ants. Urban Ecosystems 14: 135-163. (PDF)
  15. Brightwell R. J., S. B. Bambara and J. Silverman. 2010. Combined effect of hemipteran control and liquid bait on Argentine ant populations Journal of Economic Entomology. 103: 1790-1796. (PDF)
  16. Brightwell R. J., P. L. Labadie and J. Silverman. 2010. Northward expansion of the invasive Argentine ant, Linepithema humile, (Hymenoptera: Formicidae) in the eastern U.S. is constrained by winter soil temperatures. Environmental Entomology. 39: 1659-1665. (PDF)
  17. Powell B. E. and J. Silverman. 2010. Population growth of Aphis gossypii and Myzus persicae (Hemiptera: Aphididae) in the presence of Linepithema humile and Tapinoma sessile (Hymenoptera: Formicidae). Environmental Entomology. 39:1492-1499. (PDF)
  18. Powell B. E. and J. Silverman. 2010. Impact of Linepithema humile and Tapinoma sessile (Hymenoptera: Formicidae) on three natural enemies of Aphis gossypii (Hemiptera: Aphididae). Biological Control. 54: 285-291. (PDF)
  19. Rowles A. D. and J. Silverman. 2010. Argentine ant invasion associated with Loblolly pines in southeastern USA: minimal impacts but seasonally sustained. Environmental Entomology. 39: 1141-1150. (PDF)
  20. Brightwell R. J. and J. Silverman. 2010. Invasive Argentine ants reduce fitness of red maple via a mutualism with an endemic coccid.Biological Invasions. 12: 2051-2057. (PDF)
  21. Menke S.B., W. Booth, R. R. Dunn, C. Schal, E. L. Vargo and J. Silverman. 2010. Is it easy to be urban? The convergent emergence of invasive life history traits in a widespread native ant. PLoS ONE 5(2): e9194. doi:10.1371/journal.pone.0009194 (PDF)
  22. Vasquez G.M., C. Schal and J. Silverman. 2009. Colony fusion in Argentine ants is guided by worker and queen cuticular hydrocarbon profile similarity. Journal of Chemical Ecology. 35: 922-932. (PDF)
  23. Powell B.E., R.J. Brightwell and J. Silverman. 2009. Effect of an invasive and native ant on a field population of the black citrus aphid (Hemiptera: Aphididae). Environmental Entomology. 38: 1618-1625. (PDF)
  24. Rowles A.D. and J. Silverman 2009. Carbohydrate supply limits invasion of natural communities by Argentine ants. Oecologia. 161: 161-171.(PDF)
  25. Brightwell R. J. and J. Silverman 2009. Effects of honeydew-producing hemipteran denial on local Argentine ant distribution and boric acid bait performance.  Journal of Economic Entomology. 102: 1170-1174. (PDF)
  26. Vasquez G. M., C. Schal and J. Silverman. 2008. Cuticular hydrocarbons as queen adoption cues in the invasive Argentine ant. Journal of Experimental Biology. 211: 1249-1256. (PDF)
  27. Silverman J. and R. J. Brightwell. 2008. The Argentine ant: Challenges in managing an invasive unicolonial pest.  Annual Review of Entomology. 53: 231-252. (PDF)
  28. Vasquez G. M and J. Silverman. 2008. Non-nestmate conspecific acceptance and the complexity of nestmate discrimination in the Argentine ant.  Behavioral Ecology and Sociobiology. 62: 537-548.(PDF)
  29. Vasquez G. M. and J. Silverman. 2008. Intraspecific aggression and colony fusion in the Argentine ant. Animal Behaviour. 75: 583-593. (PDF)
  30. Brightwell R. J. and J. Silverman. 2007.  Argentine ant foraging activity and interspecific competition in complete vs. queenless and broodless colonies. Insectes Sociaux. 54: 329-333. (PDF)
  31. Buczkowski G. and J. Silverman. 2006. Geographic variation in Argentine ant aggression behaviour mediated by environmentally-derived nestmate recognition cues. Animal Behaviour. 71: 327-335.  (PDF)
  32. Silverman J., C.E. Sorenson and M.G. Waldvogel. 2006. Trap-mulching Argentine ants. Journal of Economic Entomology. 99: 1757-1760. (PDF)
  33. Buczkowski G., R. Kumar, S.L. Suib and J. Silverman. 2005. Diet-related modification of cuticular hydrocarbon profiles of the Argentine ant,Linepithema humile, diminishes intercolony aggression. Journal of Chemical Ecology. 31: 829-843. (PDF)
  34. Alder P. M. and J. Silverman. 2005. Effects of interspecific competition between two urban ant species, Linepithema humile andMonomorium minimum, on toxic bait performance. Journal of Economic Entomology. 98: 493-501.(PDF)
  35. Buczkowski G. and J. Silverman. 2005. Context-dependent nestmate discrimination and the effect of action thresholds on exogenous cue recognition in the Argentine ant. Animal Behaviour. 69: 741-749. (PDF)
  36. Silverman  J. 2005. The genetic basis of German cockroach bait aversion, pp. 425-426. In C.Y. Lee and W.H. Robinson [eds.], Proceedings of the fifth International Conference on Urban Pest, 10-12 July 2005, Suntec, Singapore. P&Y Design Network, Penang, Malaysia. 
  37. Silverman  J. 2005.  Why do certain ants thrive in the urban environment? In C.Y. Lee and W.H. Robinson [eds.], Proceedings of the fifth International Conference on Urban Pest, 10-12 July 2005, Suntec, Singapore. P&Y Design Network, Penang, Malaysia.
  38. Alder P. M. and J. Silverman. 2004.  A Comparison of monitoring methods used to detect changes in Argentine ant (Hymenoptera: Formicidae) populations. Journal of Agricultural and Urban Entomology. 21: 142-149.
  39. Buczkowski G., E. Vargo and J. Silverman. 2004. The diminutive supercolony: The Argentine ants of the southeastern U.S. Molecular Ecology. 13: 2235-2242. (PDF)
  40. Silverman  J. 2004. Regional distinctions in invasive Argentine ant populations. Proceedings of the 2004 National Conference on Urban Entomology.  Phoenix AZ. May, 2004.  Pg. 54.
  41. Roulston T.H., G. Buczkowski and J. Silverman. 2003. Nestmate discrimination in ants: effect of bioassay on aggressive behavior.  Insectes Sociaux. 50: 151-159. (PDF)
  42. Meissner H.E. and J. Silverman. 2003. Effect of aromatic cedar mulch on Argentine ant (Hymenoptera: Formicidae) foraging activity and nest establishment.  Journal of Economic Entomology. 96: 850-855. (PDF)
  43. Silverman J. and T. H. Roulston. 2003. Retrieval of granular bait by the Argentine ant (Hymenoptera: Formicidae): Effect of clumped vs scattered dispersion patterns. Journal of Economic Entomology. 96: 871-874. (PDF)
  44. Roulston T.H. and J. Silverman. 2002. The Effect of Food Size and Dispersion Pattern on Retrieval Rate by the Argentine ant, Linepithemahumile (Hymenoptera: Formicidae).  Journal of Insect Behavior. 15:633-648. (PDF)
  45. Meissner H. E. and J. Silverman. 2001. Effects of Aromatic Cedar Mulch on the Argentine Ant and the Odorous House Ant (Hymenoptera: Formicidae). Journal of Economic Entomology. 94: 1526-1531. (PDF)
  46. Silverman J. and T. H. Roulston. 2001.  Acceptance and intake of gel and liquid sucrose compositions by the Argentine ant (Hymenoptera: Formicidae). Journal of Economic Entomology.  94: 511-515. (PDF)
  47. Liang D., G. J. Blomquist and J. Silverman. 2001.  Hydrocarbon-induced nestmate aggression in the Argentine ant, Linepithema humile, following encounters with insect prey. Comparative Biochemistrry and Physiology Part B. 129: 871-882. (PDF)
  48. Silverman J and D. Liang. 2001.  Colony disassociation following diet partitioning in a unicolonial ant. Naturwissenshaften. 88: 73-77. (PDF)
  49. Liang D. and J. Silverman. 2000. “You are what you eat”: Diet modifies cuticular hydrocarbons and nestmate recognition in the Argentine ant, Linepithema humileNaturwissenshaften. 87: 412-416. (PDF)
  50. Silverman J. and B. Nsimba. 2000.  Soil-free collection of Argentine ants (Hymenoptera: Formicidae) based on food-directed brood and queen movement. Florida Entomologist 83: 10-16. (PDF)
  51. Silverman J. and D. N. Bieman. 2000.  Cockroach baits:  Do we have the magic bullet? Proceedings of the 2000 National Conference on Urban Entomology.  Ft. Lauderdale FL. 73-80.
  52. Silverman J. and D. Liang. 1999.  Effect of fipronil on bait formulation-based aversion in the German cockroach (Dictyoptera: Blattellidae).Journal of Economic Entomology.  92: 886-889. (PDF)
  53. Silverman J. and H. Selbach. 1998.  The behavior and survival of glucose-averse Blattella germanica provided glucose as a sole food source. Journal of Insect Behavior.  11: 93-102. (PDF)
  54. Silverman J., 1998. Studying the genetics of behavior and evolution by adaptation and natural selection.  The American Biology Teacher. 60: 356-358. (PDF)
  55. Silverman J. and D.N. Bieman. 1996.  Issues affecting the performance of cockroach baits.  International Conference on Insect Pests in the Urban Environment, 2nd Proceedings, edited by K.B. Wildey. Edinburgh, U.K.
  56. Silverman J.  1995.  Effects of glucose-supplemented diets on consumption, nymphal development, and reproduction of glucose-averse, non-glucose- averse,and heterozygous strains of the German cockroach, Blattella germanica.  Entomologia experimentalis et applicata. 76: 7-14. (PDF)
  57. Ross M.H. and J. Silverman. 1995.  Genetic studies of a behavioral mutant, glucose aversion, in the German cockroach.  Journal of Insect Behavior.  8: 825-834. (PDF)
  58. Ross M.H. and J. Silverman. 1995.  Location of the glucose aversion gene on linkage group VIII of the German cockroach (Dictyoptera: Blattellidae).  Annals of the Entomological Society of America.  88: 846-847. (PDF)
  59. Silverman J. and M.H. Ross. 1994.  Behavioral resistance of field-collected German cockroaches (Blattodea: Blattellidae) to baits containing glucose.  Environmental Entomology. 23: 425-430. (PDF)
  60. Silverman J. and A.G. Appel. 1994.  Adult cat flea (Siphonaptera: Pulicidae) excretion of host blood proteins in relation to larval nutrition. Journal of Medical Entomology. 31: 265-271. (PDF)
  61. Silverman J. and D.N. Bieman. 1993. Glucose aversion in the German cockroach, Blattella germanica. Journal of Insect Physiology. 39: 925-933.(PDF)
  62. Bieman D.N., J. Silverman, Y.R. Mehra, D.S. Lesiewicz and J. Tomeu. 1993. A sweet solution. Pest Control Technology. September: 32-36. Cover Story.
  63. Silverman J., G.I. Vitale and T.J. Shapas. 1991.  Hydramethylnon uptake by Blattella germanica (L.) via coprophagy.  Journal of Economic Entomology. 84: 176-180. (PDF)
  64. Silverman J and T.J. Shapas. 1986.  Cumulative toxicity and delayed temperature effects of hydramethylnon on German cockroaches (Orthoptera: Blattellidae).  Journal of Economic Entomology. 79: 1613-1616. (PDF)
  65. Silverman J. 1986.  Adult German cockroach (Orthoptera: Blattellidae) feeding and drinking behavior as a function of density and harborage-to-resource distance.  Environmental Entomology. 15: 198-204. (PDF)
  66. Silverman J. and M.K. Rust. 1985.  Extended longevity of the pre-emerged adult cat flea, Ctenocephalides felis, and factors stimulating emergence from the pupal cocoon.  Annals of the Entomological Society of America. 78: 763-768. (PDF)
  67. Silverman J. and A.G. Appel. 1984.  The pupal cocoon of the cat flea, Ctenocephalides felis:  A barrier to ant predation.  Proceedings of the Entomological Society of Washington 86: 660-663.
  68. Silverman J. and M.K. Rust. 1983.  Some abiotic factors limiting survival of Ctenocephalides felis.  Environmental Entomology 12: 490-495. (PDF)
  69. Silverman J., E.G. Platzer and M.K. Rust. 1982.  Infection of Ctenocephaildes felis by Neoaplectana carpocapsae.  Journal of Nematology. 14: 394-397. (PDF)
  70. Silverman J., M.K. Rust and D.A. Reierson. 1981.  Influence of temperature and humidity on the survival and development of the cat flea,Ctenocephalides felis (Siphonaptera: Pulicidae). Journal of Medical Entomology. 18: 78-83. (PDF)
  71. Rust M.K., D.A. Reierson and J. Silverman. 1981.  Insecticides to control cat flea larvae indoors.  Insecticide and Acaricide Tests. 6: 184-185.
  72. Rust M.K., D.A. Reierson and J. Silverman. 1981.  Insecticides to control adult cat fleas indoors.  Insecticide and Acaricide Tests. 6: 183-184.
  73. Silverman J., D.A. Reierson and M.K. Rust. 1980.  Insecticides for control of cat flea larvae.  Insecticide and Acaricide Tests. 5: 213-214.
  74. Silverman J. and R.D. Goeden. 1980.  Life history of a fruit fly, Procecidochares n. sp. (Diptera: Tephritidae) on the ragweed, Ambrosia dumosa, in Southern California.  Pan-Pacific Entomologist. 56: 283-288.
  75. Silverman J. and R.D. Goeden. 1979.  Life history of the lacebug Corythucha morrilli (Hemiptera: Tingidae) on the ragweed, Ambrosia dumosa, in Southern California.  Pan-Pacific Entomologist. 56: 283-288.
  76. Silverman J., D.A. Reierson and M.K. Rust. 1979.  Insecticides for cat flea control.  Insecticide and Acaricide Tests. 4: 206.

Dr. Silverman in "Perspectives" magazine