Abstract
Female-released chemical signals are crucial clues for mate-searching males to locate and gain sexual receptivity of conspecific females. Abundant behavioral evidence indicates that female spiders release sex pheromones to guide mate-searching behavior of conspecific mature males. However, the chemical nature of spider pheromones is poorly understood. Females of the funnel-web spider, Allagelena difficilis, employ sit-and-wait tactics for mating. Field observations indicate that males leave their retreats to search for potential mates during the breeding season. Therefore, we investigated whether virgin females release a sex attractant to conspecific males and then explored the chemical nature of the female pheromone. Four fatty acids extracted from the female bodies (palmitic acid, linoleic acid, cis-vaccenic acid and stearic acid) constitute a multiple-component sex attractant to conspecific males in A. difficilis. Unexpectedly, mated females also produce the same fatty acids, but at trace levels. Two-choice experiments showed that males were significantly attracted by the blend of the four fatty acids in appropriate concentrations while avoiding the blend consisting of the same acids at very low concentrations, suggesting that mate-searching males are able to discriminate virgin females from mated females by the quantities of female-specific fatty acids in the funnel-web spider A. difficilis.
Similar content being viewed by others
References
Barth FG (2002) A Spider's world. Senses and behavior. Springer-Verlag, Berlin Heidelberg. https://doi.org/10.1007/978-3-662-04899-3
Baruffaldi L, Andrade MCB (2015) Contact pheromones mediate male preference in black widow spiders: avoidance of hungry sexual cannibals? Anim Behav 102:25–32. https://doi.org/10.1016/j.anbehav.2015.01.007
Bell RD (2015) The Role of Pheromones in the Sexual Communication of the Wolf Spider, Schizocosa ocreata (Araneae, Lycosidae), Ohio State University and OhioLINK. Dissertation, The Ohio State University
Chinta SP, Goller S, Lux J, Funke S, Uhl G, Schulz S (2010) The sex pheromone of the wasp spider Argiope bruennichi. Angew Chem Int Ed 49:2033–2036. https://doi.org/10.1002/anie.200906311
Chinta SP, Goller S, Uhl G, Schulz S (2016) Identification and synthesis of branched wax-type esters, novel surface lipids from the spider Argyrodes elevatus (Araneae: Theridiidae). Chem Biodivers 13:1202–1220. https://doi.org/10.1002/cbdv.201600020
Cory AL, Schneider JM (2016) Old maids have more appeal: effects of age and pheromone source on mate attraction in an orb-web spider. Peerj 4:e1877. https://doi.org/10.7717/peerJ.1877
Foelix RF (2011) Biology of spiders, 3rd edn. Oxford University Press, New York
Gaskett AC (2007) Spider sex pheromones: emission, reception, structures, and functions. Biol Rev 82:27–48. https://doi.org/10.1111/j.1469-185X.2006.00002.x
Henneken J, Goodger JQD, Jones TM, Elgar MA (2017) Diet-mediated pheromones and signature mixtures can enforce signal reliability. Front Ecol Evol 4:e145. https://doi.org/10.3389/fevo.2016.00145
Jerhot E, Stoltz JA, Schulz S (2010) Acylated serine derivatives: a unique class of arthropod pheromones of the Australian redback spider, Latrodectus hasselti. Angew Chem Int Ed 49:2037–2040. https://doi.org/10.1002/anie.200906312
Nelson XJ, Warui CM, Jackson RR (2012) Widespread reliance on olfactory sex and species identification by lyssomanine and spartaeine jumping spiders. Biol J Linn Soc 107:664–677. https://doi.org/10.1111/j.1095-8312.2012.01965.x
Papke M, Schulz S, Tichy H, Gingl E, Ehn R (2000) Identification of a new sex pheromone from the silk dragline of the tropical wandering spider Cupiennius salei. Angew Chem Int Ed 39:4339–4341. https://doi.org/10.1002/chin.200112230
Papke MD, Riechert SE, Schulz S (2001) An airborne female pheromone associated with male attraction and courtship in a desert spider. Anim Behav 61:877–886. https://doi.org/10.1006/anbe.2000.1675
Pourié G, Ibarra F, Francke W, Trabalon M (2005) Fatty acids mediate aggressive behavior in the spider Tegenaria atrica. Chemoecol 15:161–166. https://doi.org/10.1007/s00049-005-0308-6
Prouvost O, Trabalon M, Papke M, Schulz S (1999) Contact sex signals on web and cuticle of Tegenaria atrica (Araneae, Agelenidae). Arch Insect Biochem Physiol 40:194–202. https://doi.org/10.1002/(SICI)1520-6327(1999)40:4<194::AID-ARCH4>3.0.CO;2-P
Schulz S (2013) Spider pheromones - a structural perspective. J Chem Ecol 39:1–14. https://doi.org/10.1007/s10886-012-0231-6
Schulz S, Toft S (1993) Identification of a sex pheromone from a spider. Science 260:1635–1637. https://doi.org/10.1126/science.260.5114.1635
Scott C, Mccann S, Gries R, Khaskin G, Gries G (2015) N-3-methylbutanoyl-O-methylpropanoyl-L-serine methyl ester–pheromone component of western black widow females. J Chem Ecol 41:465–472. https://doi.org/10.1007/s10886-015-0582-x
Scott C, Gerak C, Mccann S, Gries G (2018) The role of silk in courtship and chemical communication of the false widow spider, Steatoda grossa (Araneae: Theridiidae). J Ethol 36:191–197. https://doi.org/10.1007/s10164-017-0539-3
Shahandeh MP, Pischedda A, Turner TL (2018) Male mate choice via cuticular hydrocarbon pheromones drives reproductive isolation between Drosophila species. Evolution 72:123–135. https://doi.org/10.1111/evo.13389
Tichy H, Gingl E, Ehn R, Papke M, Schulz S (2001) Female sex pheromone of a wandering spider (Cupiennius salei): identification and sensory reception. J Comp Physiol A - Sensory Neural Behav Physiol 187:75–78. https://doi.org/10.1007/s003590000175
Trabalon M (2013) Chemical communication and contact cuticular compounds in spiders. In: Nentwig W (ed) Spider Ecophysiology. Springer-Verlag Berlin Heidelberg, Berlin Heidelberg, pp 125–140. https://doi.org/10.1007/978-3-642-33989-9_10
Trabalon M, Niogret J, Legrand-Frossi C (2005) Effect of 20-hydroxyecdysone on cannibalism, sexual behavior, and contact sex pheromone in the solitary female spider, Tegenaria atrica. Gen Comp Endocrinol 144:60. https://doi.org/10.1016/j.ygcen.2005.04.011
Wyatt TD (2014) Pheromones and animal behaviour: chemical signals and signatures, 2nd edn. Cambridge University Press, Cambridge
Xiao YH, Zhang JX, Li SQ (2009) A two-component female-produced pheromone of the spider Pholcus beijingensis. J Chem Ecol 35:769–778. https://doi.org/10.1007/s10886-009-9660-2
Xiao YH, Zhang JX, Li SQ, (2010) Male-specific (Z)-9-tricosene stimulates female mating behaviour in the spider Pholcus beijingensis. Proc R Soc B Biol Sci 277:3009–3018. https://doi.org/10.1098/rspb.2010.0763
Xiao YH, Zunic-Kosi A, Zhang LW, Prentice TR, Mcelfresh JS, Chinta, SP, Zou YF, Millar JG (2015) Male adaptations to minimize sexual cannibalism during reproduction in the funnel-web spider Hololena curta. Insect Sci 22:840–852. https://doi.org/10.1111/1744-7917.12243
Acknowledgments
This work was funded by the Natural Sciences Foundation of China (NSFC 31560592, 31471963, 31772423) and the Science and Technology Foundation of Jiangxi Provincial Department of Education (GJJ160753). We thank Zeyuan Meng, Wenjun Xie (College of Life Sciences, Jinggangshan University, China) for collecting spiders with the authors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Chen, ZW., Zhao, YF., He, SC. et al. Particular Levels of Odors Released by Virgin Females Attract Conspecific Males of the Funnel-Web Spider Allagelena difficilis. J Chem Ecol 44, 905–914 (2018). https://doi.org/10.1007/s10886-018-0998-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-018-0998-1