Longhorned beetles (Coleoptera: Cerambycidae) include many species that are among the most damaging pests of managed and natural forest ecosystems worldwide. Many species of cerambycids use volatile chemical signals (i.e., pheromones) to locate mates. Pheromones are often used by natural enemies, including parasitoids, to locate hosts and therefore can be useful tools for identifying host-parasitoid relationships. In two field experiments, we baited linear transects of sticky traps with pheromones of cerambycid beetles in the subfamily Cerambycinae. Enantiomeric mixtures of four linear alkanes or four linear alkanes and a ketol were tested separately to evaluate their attractiveness to hymenopteran parasitoids. We hypothesized that parasitoids would be attracted to these pheromones. Significant treatment effects were found for 10 species of parasitoids. Notably, Wroughtonia ligator (Say) (Hymenoptera: Braconidae) was attracted to syn-hexanediols, the pheromone constituents of its host, Neoclytus acuminatus acuminatus (F.) (Coleoptera: Cerambycidae). Location and time of sampling also significantly affected responses for multiple species of parasitoids. These findings contribute to the basic understanding of cues that parasitoids use to locate hosts and suggest that pheromones can be used to hypothesize host relationships between some species of cerambycids and their parasitoids. Future work should evaluate response by known species of parasitoids to the complete blends of pheromones used by the cerambycids they attack, as well as other odors that are associated with host trees of cerambycids.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Dataset is available upon request from first author, T.D. Johnson.
Aukema JE, Leung B, Kovacs K, Chivers C, Britton KO, Englin J, Frankel SJ, Haight RG, Holmes TP, Liebhold AM, McCullough DG, Von Holle B (2011) Economic impacts of non-native forest insects in the continental United States. PLoS One 6:e24587
Bretz F, Hothorn T, Westfall P (2010) Multiple comparisons using R. CRC Press, Boca Raton
Brues CT (1922) Some hymenopterous parasites of lignicolous Itonididae. Proc Am Acad Arts Sci 57:263–289
Buffington ML, Polaszek A (2009) Recent occurrence of Aphanogmus dictynna (Waterson) (Hymenoptera: Ceraphronidae) in Kenya – an important hyperparasitoid of the coffee berry borer Hypothenemus hampei (Ferrari) (Coleoptera: Curculionidae). Zootaxa 2214:62–68
Cardé RT (2014) Defining attraction and aggregation pheromones: teleological versus functional perspectives. J Chem Ecol 40:519–520
Champlain AB (1922) Records of hymenopterous parasites in Pennsylvania. Psyche 29:95–100
Collignon RM, Swift IP, Zou Y, McElfresh JS, Hanks LM, Millar JG (2016) The influence of host plant volatiles on the attraction of longhorn beetles to pheromones. J Chem Ecol 42:215–229
Duan JJ, Aparicio E, Tatman D, Smith MT, Luster DG (2015) Potential new associations of north American parasitoids with the invasive Asian longhorned beetle (Coleoptera: Cerambycidae) for biological control. J Econ Entomol 109:699–704
Eyre D, Haack RA (2017) Invasive cerambycid pests and biosecurity measures. In: Wang Q (ed) Cerambycidae of the world: biology and pest management. CRC Press/Taylor & Francis, Boca Raton, pp 563–618
Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689
Fox J, Weisberg S (2011) A companion to applied regression, 2nd edn. Sage, Thousand Oaks
Gardiner LM (1960) Descriptions of immature forms and biology of Xylotrechus colonus (fab.) (Coleoptera: Cerambycidae). Can Entomol 92:820–825
Gibson GAP, Huber JT, Woolley JB (eds) (1997) Annotated keys to the genera of Nearctic Chalcidoidea (Hymenoptera). NRC Research Press, Ottawa
Golec JR, Aparicio E, Wang X, Duan JJ, Fuester RW, Tatman D, Kula RR (2020) Cerambycid communities and their associated hymenopteran parasitoids from major hardwood trees in Delaware: implications for biocontrol of invasive longhorned beetles. Environ Entomol 49:370–382
Greathead DJ (1963) A review of the insect enemies of Acridoidea (Orthoptera). Trans R Entomol Soc Lond 114:437–523
Grebennikov VV, Gill BD, Vigneault R (2010) Trichoferus campestris (Faldermann) (Coleoptera: Cerambycidae), an Asian wood-boring beetle recorded in North America. Coleopt Bull 64:13–20
Haack RA, Hérard F, Sun J, Turgeon JJ (2010) Managing invasive populations of Asian longhorned beetle and citrus longhorned beetle: a worldwide perspective. Annu Rev Entomol 55:521–546
Hanks LM, Gould JR, Paine TD, Millar JG, Wang Q (1995) Biology and host relations of Avetianella longoi (Hymenoptera: Encyrtidae), an egg parasitoid of the eucalyptus longhorned borer (Coleoptera: Cerambycidae). Ann Entomol Soc Am 88:666–671
Hanks LM, Reagel PF, Mitchell RF, Wong JCH, Meier LR, Silliman CA, Graham EE, Striman BL, Robinson KP, Mongold-Diers JA, Millar JG (2014) Seasonal phenology of the cerambycid beetles of east-Central Illinois. Ann Entomol Soc Am 107:211–226
Hanks LM, Millar JG (2016) Sex and aggregation-sex pheromones of cerambycid beetles: basic science and practical applications. J Chem Ecol 42:631–654
Hanks LM, Wang Q (2017) Reproductive biology of cerambycids. In: Wang Q (ed) Cerambycidae of the world: biology and pest management. CRC Press/Taylor & Francis, Boca Raton, pp 133–159
Hanks LM, Mongold-Diers JA, Atkinson TH, Fierke MK, Ginzel MD, Graham EE, Poland TM, Richards AB, Richardson ML, Millar JG (2018) Blends of pheromones, with and without host plant volatiles, can attract multiple species of cerambycid beetles simultaneously. J Econ Entomol 111:716–724
Hassanali A, Njagi PGN, Bashir MO (2005) Chemical ecology of locusts and related acridids. Annu Rev Entomol 50:223–245
Hauck WW, Donner A (1977) Wald’s test as applied to hypotheses in logit analysis. J Am Stat Assoc 72:851–853
Heraty J, Hawks D (1998) Hexamethyldisilazane – a chemical alternative for drying insects. Entomol News 109:369–374
Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363
Jurc M, Csóka G, Hrašovec B (2016) Potentially important insect pests of Celtis australis in Slovenia, Crotia, and Hungary. Šumar list 11–12:577–588
Johnson TD, Lelito JP, Raffa KF (2014) Responses of two parasitoids, the exotic Spathius agrili Yang and the native Spathius floridanus Ashmead, to volatile cues associated with the emerald ash borer. Agrilus planipennis Fairmaire 79:110–117
Keeling CO, Plettner E, Slessor KN (2004) Hymenopteran semiochemicals. Top Curr Chem 239:133–177
Kosmidis I (2017) brglm: Bias reduction in binary-response generalized linear models. R package version 0.6.1, http://www.ucl.ac.uk/~ucakiko/software.html
Lindenmayer DB, Noss RF (2006) Salvage logging, ecosystem processes, and biodiversity conservation. Conser Biol 20:949–958
Masner L (1976) Revisionary notes and keys to world genera of Scelionidae (Hymenoptera: Proctotrupoidea). Mem Entomol Soc Can 97:1–87
Masner L, Huggert L (1989) World review and keys to genera of the subfamily Inostemmatinae with reassignment of the taxa to the Platygastrinae and Sceliotrachelinae (Hymenoptera: Platygastridae). Mem Entomol Soc Can 147:1–214
Mattiacci L, Vinson SB, Williams HJ, Aldrich JR, Bin F (1993) A long-range attractant kairomone for egg parasitoid Trissolcus basalis, isolated from defensive secretion of its host, Nezara viridula. J Chem Ecol 19:1167–1181
McKenna DD, Scully ED, Pauchet Y et al (2016) Genome of the Asian longhorned beetle (Anoplophora glabripennis), a globally significant invasive species, reveals key functional and evolutionary innovations at the beetle-plant interface. Genome Biol 17:227
Meiners T, Peri E (2013) Chemical ecology of insect parasitoids: essential elements for developing effective biological control programs. In: Wajnberg E, Colazza S (eds) Chemical ecology of insect parasitoids. Wiley, Chichester, pp 193–224
Millar JG, Hanks LM (2017) Chemical ecology of cerambycids. In: Wang Q (ed) Cerambycidae of the world: biology and pest management. CRC Press/Taylor & Francis, Boca Raton, pp 161–208
Millar JG, Richards AB, Halloran S, Zou Y, Boyd EA, Quigley KN, Hanks LM (2019) Pheromone identification by proxy: identification of aggregation-sex pheromones of north American cerambycid beetles as a strategy to identify pheromones of invasive Asian congeners. J Pest Sci 92:213–220
Miller DR, Crowe CM, Mayo PD, Silk PJ, Sweeney JD (2015) Responses of Cerambycidae and other insects to traps baited with ethanol, 2,3-hexanediol, and 3,2-hydroxyketone lures in north-Central Georgia. J Econ Entomol 108:2354–2365
Nowak DJ, Pasek JE, Sequeira RA, Crane DE, Mastro VC (2001) Potential effect of Anoplophora glabripennis (Coleoptera: Cerambycidae) on urban trees in the United States. J Econ Entomol 94:116–122
Noyes JS (2018) Universal Chalcidoidea Database. http://www.nhm.ac.uk/chalcidoids
Paine TD, Millar JG, Hanks LM, Gould J, Wang Q, Danne K, Dahlsten DL, McPherson EG (2015) Cost-benefit analysis for biological control programs that targeted insect pests of eucalypts in urban landscapes of California. J Econ Entomol 108:2497–2504
Pearse IS, Gee WS, Beck JJ (2013) Headspace volatiles from 52 oak species advertise induction, species identity, and evolution, but not defense. J Chem Ecol 39:90–100
Perry KI, Herms DA (2019) Dynamic responses of ground-dwelling invertebrate communities to disturbance in forest ecosystems. Insects 10:61
Pfammatter JA, Krause A, Raffa KF (2015) Evaluating predators and competitors in Wisconsin red pine forests for attraction to mountain pine beetle pheromones for anticipatory biological control. Environ Entomol 44:1161–1171
Quicke DLJ (2015) Idiobionts, koinobionts and other life history traits. In: DLJ Q (ed) The braconid and ichneumonid parasitoid wasps, 1st edn. Wiley, New York, pp 87–106
Raffa KF, Klepzig KD (1989) Chiral escape of bark beetles from predators responding to a bark beetle pheromone. Oecologia 80:566–569
Ray AM, Millar JG, Moreira JA, McElfresh JS, Mitchell RF, Barbour JD, Hanks LM (2015) North American species of cerambycid beetles in the genus share a common hydroxyhexanone-hexanediol pheromone structural motif. J Econ Entomol 108:1860–1868
R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reagel PF, Smith MT, Hanks LM (2012) Effects of larval host diameter on body size, adult density, and parasitism of cerambycid beetles. Can Entomol 144:1–4
Rhainds M, Heard SB, Hughes C, Mackinnon W, Porter W, Sweeney J, Silk P, Demerchant I, McClean S, Brodersen G (2015) Evidence for mate-encounter Allee effect in an invasive longhorn beetle (Coleoptera: Cerambycidae). Ecol Entomol 40:829–832
Rutledge CE (1996) A survey of identified kairomones and synomones used by insect parasitoids to locate and accept their hosts. Chemoecol 7:121–131
Smith MT, Turgeon JJ, De Groot P, Gasman B (2009) Asian Longhorned beetle Anoplophora glabripennis (Motschulsky): lessons learned and opportunities to improve the process of eradication and management. Am Entomol 55:21–25
Solomon JD (1995) Agriculture handbook 706: guide to insect borers of north American broadleaf trees and shrubs. USDA Forest Service, Washington
Sullivan DJ, Völkl W (1999) Hyperparasitism: multitrophic ecology and behavior. Annu Rev Entomol 44:291–315
U.S. Department of Agriculture–Animal and Plant Health Inspection Service (USDA-APHIS) (2015) Asian Longhorned Beetle Eradication Program. (http://www.regulations.gov/#!documentDetail;D=APHIS-2013-0003- 0029) (accessed 19 February 2019)
Van Driesche RG, Carruthers RI, Center T, Hoddle MS, Hough-Goldstein J, Morin L, Smith DL et al (2010) Classical biological control for the protection of natural ecosystems. Biol Control 54:S2–S33
Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Annu Rev Entomol 37:141–172
Walde SJ, Murdoch WW (1988) Spatial density dependence in parasitoids. Annu Rev Entomol 33:441–466
Wang Q, Millar JG, Reed DA, Mottern JL, Heraty JM, Triapitsyn SV, Paine TD, He XZ (2008) Development of a strategy for selective collection of a parasitoid attacking one member of a large herbivore guild. J Econ Entomol 101:1771–1778
Wiskerke JSC, Dicke M, Vet LEM (1993) Larval parasitoid uses aggregation pheromone of adult hosts in foraging behaviour: a solution to the reliability-detectability problem. Oecologia 93:145–148
Wong JCH, Meier LR, Zou Y, Mongold-Diers JA, Hanks LM (2017) Evaluation of methods used in testing attraction of cerambycid beetles to pheromone-baited traps. J Econ Entomol 110:2269–2274
Yanega D (1996) Field guide to northeastern longhorned beetles (Coleoptera: Cerambycidae), manual 6. Illinois Natural History Survey, Champaign, IL
Yu DSK, van Achterberg C, Horstmann K (2016) Taxapad 2016 –world Ichneumonoidea 2015. Taxonomy, biology, morphology and distribution. Nepean, Ontario, Canada. (http://www.taxapad. Com)
Zeileis A, Kleiber C, Jackman S (2008) Regression models for count data in R. J Stat Softw 27:1–25
Zuk M, Kolluru GR (1998) Exploitation of sexual signals by predators and parasitoids. Q Rev Biol 73:415–438
Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York
We thank Jocelyn G. Millar for the gift of the four alkanediols used in our study and Judith Mongold-Diers for general assistance in the lab. For assistance with removal of parasitoids from traps, we thank undergraduate technicians Emily Althoff, Briana Banks, Elizabeth Hanson, Kaleb Lukens, Nicholas Mendes, Julia Monk, Kaylynn Pingad, Suzanne Vachula, Brian Willis, and Allen Yu. John S. Noyes provided assistance with the identification of some Encrytidae. Statistical advice was provided by Ben Bolker on Stackoverflow. This manuscript was improved by comments from Brian Allan, May Berenbaum, Lawrence M. Hanks, István Mikó, Robert F. Mitchell, Andrew Suarez, and an anonymous reviewer. Our experiment was funded by support from United States Department of Agriculture National Institute of Food and Agriculture grant number 2012-67013-19303 and the Alphawood Foundation of Chicago (to Lawrence M. Hanks and Jocelyn G. Millar). Elijah Talamas was supported by the Florida Department of Agriculture and Consumer Services, Division of Plant Industry. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer.
Our experiment was funded by support from United States Department of Agriculture National Institute of Food and Agriculture grant number 2012–67013-19303 and the Alphawood Foundation of Chicago. Elijah Talamas was supported by the Florida Department of Agriculture and Consumer Services, Division of Plant Industry.
Conflict of Interest
We have no conflicts of interest to report.
This manuscript was approved for submission by the Florida Department of Agriculture and Consumer Services, Division of Plant Industry, and the USDA Agricultural Research Service Systematic Entomology Laboratory.
Consent to Participate
All authors consented to participate in their respective roles for this study.
Consent for Publication
All authors consented to submitting this manuscript for publication.
R code for analyses is available upon request from first author, T.D. Johnson.
About this article
Cite this article
Johnson, T.D., Buffington, M.L., Gates, M.W. et al. Deployment of Aggregation-Sex Pheromones of Longhorned Beetles (Coleoptera: Cerambycidae) Facilitates the Discovery and Identification of their Parasitoids. J Chem Ecol 47, 28–42 (2021). https://doi.org/10.1007/s10886-020-01238-7
- Host location
- Neoclytus acuminatus
- Wroughtonia ligator