Journal of Chemical Ecology

, Volume 44, Issue 2, pp 189–197 | Cite as

Feminization of Male Brown Treesnake Methyl Ketone Expression via Steroid Hormone Manipulation

  • M. Rockwell ParkerEmail author
  • Saumya M. Patel
  • Jennifer E. Zachry
  • Bruce A. Kimball


Pheromones are useful tools for the management of invasive invertebrates, but have proven less successful in field applications for invasive vertebrates. The brown treesnake, Boiga irregularis, is an invasive predator that has fundamentally altered the ecology of Guam. The development of control tools to manage Boiga remains ongoing. Skin-based, lipophilic pheromone components facilitate mating in brown treesnakes, with females producing the same long-chain, saturated and monounsaturated (ketomonoene) methyl ketones known to function as pheromones in garter snakes, Thamnophis sirtalis. Boiga also express novel, diunsaturated methyl ketones (ketodienes) with a purported function as a sex pheromone. In our study, we implanted 17 β-estradiol in adult male brown treesnakes in order to manipulate methyl ketone expression as sex attractants, an effect that would mirror findings with garter snakes. Specifically, estrogen promoted production of two ketomonoenes, pentatriaconten-2-one and hexatriaconten-2-one, and suppressed production of one ketodiene, heptatriacontadien-2-one. In bioassays, estrogen-implanted males elicited tongue-flicking and chin rubbing behavior from unmanipulated males, though the responses were weaker than those elicited by females. On Guam, wild males exhibited greatest responses to whole female skin lipid extracts and only weak responses to the methyl ketone fractions from females and implanted males. Our results suggest that sex identity in brown treesnakes may be conferred by the ratio of ketomonoenes (female) to ketodienes (male) from skin lipids and may be augmented by a sex-specific endocrine signal (estradiol). However, a blend of long-chain methyl ketones alone is not sufficient to elicit maximal reproductive behaviors in male Boiga.


Pheromone Estrogen Snake Boiga Reproduction Invasive species 



G. Gathright (U.S. Department of Agriculture [USDA], National Wildlife Research Center [NWRC]) conducted the implantation surgeries. J. Noll and S. Ashton-Cromwell assisted with fractionation of samples at James Madison University (JMU). The project was funded primarily by an agreement between the USDA NWRC and Washington and Lee University (WLU)(14-7483-1088-CA) and more recently by an agreement between USDA NWRC and JMU (16-7442-1225-CA), made possible by funding from the Department of Defense Joint Regions Marianas (N61128-14-MP-001AG). MRP and SMP were supported by funding from an HHMI institutional grant (WLU), and MRP also received a partial grant from the Lenfest Foundation of WLU and a faculty summer research supplement from the College of Science and Mathematics (JMU). GC/MS analysis was conducted at the Roy J. Carver Biotechnology Center at the University of Illinois, with significant assistance from A. Ulanov. Bioassays on Guam were made possible through field collections and animal care provided by C. Robinson and M. Viernes of the U.S. Geological Survey (USGS). A. Bristol, L. Moore, and A. Narzynski assisted with very late-night bioassays. All Guam work was initiated and coordinated by E. Holldorf and R. Reed (USGS), with special thanks to J. Savidge (Colorado State University). All procedures involving the use of vertebrate animals were approved by the IACUC of the USDA NWRC (QA-2339) and USGS (2016-10). The manuscript and figures were improved following helpful critiques by three anonymous reviewers.


  1. Albajes R, Konstantopoulou M, Etchepare O, Eizaguirre M, Frérot B, Sans A, Krokos F, Améline A, Mazomenos B (2002) Mating disruption of the corn borer Sesamia nonagrioides (Lepidoptera: Noctuidae) using sprayable formulations of pheromone. Crop Prot 21:217–225. CrossRefGoogle Scholar
  2. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  3. Bohnenblust EW, Breining JA, Shaffer JA, Fleischer SJ, Roth GW, Tooker JF (2014) Current European corn borer, Ostrinia nubilalis, injury levels in the northeastern United States and the value of Bt field corn. Pest Manag Sci 70:1711–1719. CrossRefPubMedGoogle Scholar
  4. Clarke GS, Crossland MR, Shine R (2016) Can we control the invasive cane toad using chemicals that have evolved under intraspecific competition? Ecol Appl 26:463–474. CrossRefPubMedGoogle Scholar
  5. El-Sayed AM, Suckling DM, Wearing CH, Byers JA (2006) Potential of mass trapping for long-term pest management and eradication of invasive species. J Econ Entomol 99:1550–1564. CrossRefPubMedGoogle Scholar
  6. Engeman RM, Vice DS (2001) Objectives and integrated approaches for the control of brown tree snakes. Integr Pest Manag Rev 6:59–76. CrossRefGoogle Scholar
  7. Gaston LK, Shorey HH, Saario CA (1967) Insect population control by the use of sex pheromones to inhibit orientation between the sexes. Nature 213:1155. CrossRefGoogle Scholar
  8. Greene MJ, Mason RT (1998) Chemically mediated sexual behavior of the brown tree snake, Boiga irregularis. Ecoscience 5:405–409. CrossRefGoogle Scholar
  9. Greene MJ, Mason RT (2000) Courtship, mating, and male combat of the brown tree snake, Boiga irregularis. Herpetologica 56:166–175Google Scholar
  10. Greene MJ, Mason RT (2003) Pheromonal inhibition of male courtship behaviour in the brown tree snake, Boiga irregularis: a mechanism for the rejection of potential mates. Anim Behav 65:905–910. CrossRefGoogle Scholar
  11. Greene MJ, Stark SL, Mason RT (2001) Pheromone trailing behavior of the brown tree snake, Boiga irregularis. J Chem Ecol 27:2193–2201. CrossRefPubMedGoogle Scholar
  12. Hwang S-Y, Lindroth RL (1997) Clonal variation in foliar chemistry of aspen: effects on gypsy moths and forest tent caterpillars. Oecologia 111:99–108. CrossRefPubMedGoogle Scholar
  13. Johnson NS, Tix JA, Hlina BL, Wagner CM, Siefkes MJ, Wang H, Li W (2015) A sea lamprey (Petromyzon marinus) sex pheromone mixture increases trap catch relative to a single synthesized component in specific environments. J Chem Ecol 41:311–321. CrossRefPubMedGoogle Scholar
  14. Kimball BA, Stelting SA, McAuliffe TW, Stahl RS, Garcia RA, Pitt WC (2016) Development of artificial bait for brown treesnake suppression. Biol Invasions 18:359–369. CrossRefGoogle Scholar
  15. LeMaster MP, Mason RT (2002) Variation in a female sexual attractiveness pheromone controls male mate choice in garter snakes. J Chem Ecol 28:1269–1285. CrossRefPubMedGoogle Scholar
  16. Mason RT (1992) Reptilian pheromones. In: Gans C, Crews D (eds) Biology of the Reptilia, vol 18. University of Chicago Press, Chicago, pp 114–228Google Scholar
  17. Mason RT, Crews D (1985) Female mimicry in garter snakes. Nature 316:59–60. CrossRefPubMedGoogle Scholar
  18. Mason RT, Parker MR (2010) Social behavior and pheromonal communication in reptiles. J Comp Physiol A 196:729–749. CrossRefGoogle Scholar
  19. Mason RT, Chinn JW, Crews D (1987) Sex and seasonal differences in the skin lipids of garter snakes. Comp Biochem Physiol B 87:999–1003. CrossRefPubMedGoogle Scholar
  20. Mason RT, Fales HM, Jones TH, Pannell LK, Chinn JW, Crews D (1989) Sex pheromones in snakes. Science 245:290–293. CrossRefPubMedGoogle Scholar
  21. Mason RT, Jones TH, Fales HM, Pannell LK, Crews D (1990) Characterization, synthesis, and behavioral responses to sex attractiveness pheromones of red-sided garter snakes (Thamnophis sirtalis parietalis). J Chem Ecol 16:2353–2369. CrossRefPubMedGoogle Scholar
  22. Mathies T, Miller LA (2003) Cool temperatures elicit reproduction in a biologically invasive predator, the brown treesnake (Boiga irregularis). Zoo Biol 22:227–238. CrossRefGoogle Scholar
  23. Mathies T, Levine B, Engeman R, Savidge JA (2013) Pheromonal control of the invasive brown treesnake: potency of female sexual attractiveness pheromone varies with ovarian state. Int J Pest Manage 59:141–149. CrossRefGoogle Scholar
  24. McNeil JN (1991) Behavioral ecology of pheromone-mediated communication in moths and its importance in the use of pheromone traps. Annu Rev Entomol 36:407–430. CrossRefGoogle Scholar
  25. Mortensen HS, Dupont YL, Olesen JM (2008) A snake in paradise: disturbance of plant reproduction following extirpation of bird flower-visitors on Guam. Biol Conserv 141:2146–2154. CrossRefGoogle Scholar
  26. Murata Y, Yeh HJ, Pannell LK, Jones TH, Fales HM, Mason RT (1991) New ketodienes from the integumental lipids of the Guam brown tree snake, Boiga irregularis. J Nat Prod 54:233–240. CrossRefPubMedGoogle Scholar
  27. Musso AE, Gries R, Zhai H, Takács S, Gries G (2017) Effect of male house mouse pheromone components on behavioral responses of mice in laboratory and field experiments. J Chem Ecol 43:215–224. CrossRefPubMedGoogle Scholar
  28. Parker MR, Mason RT (2009) Low temperature dormancy affects the quantity and quality of the female sexual attractiveness pheromone in red-sided garter snakes. J Chem Ecol 35:1234–1241. CrossRefPubMedGoogle Scholar
  29. Parker MR, Mason RT (2011) Pheromones in snakes: history, patterns and future research directions. In: Aldridge RD, Sever DM (eds) Reproductive biology and phylogeny of snakes. CRC Press, Boca Raton, pp 551–572CrossRefGoogle Scholar
  30. Parker MR, Mason RT (2012) How to make a sexy snake: estrogen activation of female sex pheromone in male red-sided garter snakes. J Exp Biol 215:723–730. CrossRefPubMedGoogle Scholar
  31. Parker MR, Mason RT (2014) A novel mechanism regulating a sexual signal: the testosterone-based inhibition of female sex pheromone expression in garter snakes. Horm Behav 66:509–516. CrossRefPubMedGoogle Scholar
  32. Reardon RC, Leonard D, Mastro V, Leonhardt B, Mclane W, Talley S, Thorpe K, Webb R (1998) Using mating disruption to manage gypsy moth: a review. USDA Forest Service, Washington, D.C.Google Scholar
  33. Rodda GH, Fritts TH (1992) The impact of the introduction of the colubrid snake Boiga irregularis on Guam's lizards. J Herpetol 26:166–174. CrossRefGoogle Scholar
  34. Rogers HS, Buhle ER, HilleRisLambers J, Fricke EC, Miller RH, Tewksbury JJ (2017) Effects of an invasive predator cascade to plants via mutualism disruption. Nat Commun 8:14557. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Saunders G, Cooke B, McColl K, Shine R, Peacock T (2010) Modern approaches for the biological control of vertebrate pests: an Australian perspective. Biol Control 52:288–295. CrossRefGoogle Scholar
  36. Savidge JA (1987) Extinction of an island forest avifauna by an introduced snake. Ecology 68:660–668. CrossRefGoogle Scholar
  37. Smith JB, Turner KL, Beasley JC, DeVault TL, Pitt WC, Rhodes OE (2016) Brown tree snake (Boiga irregularis) population density and carcass locations following exposure to acetaminophen. Ecotoxicology 25:1556–1562. CrossRefPubMedGoogle Scholar
  38. Takács S, Gries R, Zhai H, Gries G (2016) The sex attractant pheromone of male brown rats: identification and field experiment. Angew Chem Int Ed 55:6062–6066. CrossRefGoogle Scholar
  39. Takács S, Gries R, Gries G (2017) Sex hormones function as sex attractant pheromones in house mice and brown rats. Chembiochem 18:1391–1395. CrossRefPubMedGoogle Scholar
  40. Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216. CrossRefPubMedGoogle Scholar
  41. Uhrig EJ, LeMaster MP, Mason RT (2014) Species specificity of methyl ketone profiles in the skin lipids of female garter snakes, genus Thamnophis. Biochem Syst Ecol 53:51–58. CrossRefGoogle Scholar
  42. Wiles GJ, Bart J, Beck RE, Aguon CF (2003) Impacts of the brown tree snake: patterns of decline and species persistence in Guam's avifauna. Conserv Biol 17:1350–1360. CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyJames Madison UniversityHarrisonburgUSA
  2. 2.Department of BiologyWashington and Lee UniversityLexingtonUSA
  3. 3.U.S. Department of Agriculture, National Wildlife Research CenterMonell Chemical Senses CenterPhiladelphiaUSA

Personalised recommendations