Does silk mediate chemical communication between the sexes in a nuptial feeding spider?

Abstract

Chemical signals play a crucial role in reproduction as a means for locating mates and/or gaining information about their quality, ultimately affecting mating system dynamics and mate choice. In spiders, one of the potential sources of chemical signalling is silk. However, while female silk is known to attract mates and/or elicit courtship, due to sex-specific roles in mate searching, male silk-related signals are often neglected. In the hunting spider Pisaura mirabilis (Pisauridae), both sexes leave silk draglines during movements while males additionally use silk to wrap nuptial gifts (food donations to females at mating). We explored the potential for both silk types (draglines and gift silk) to release signals and tested the hypothesis that chemical compounds bound to gifts’ silk serve to elicit female attraction. We conducted behavioural choice assays for dragline and gift silk, and their putative transmission mode (airborne or contact) by testing (i) male and female attraction towards draglines of the opposite sex and (ii) female attraction towards gift silk. Whereas males were attracted to female draglines (contact cues), females did not respond to male silk of any type. We suggest that females use draglines for advertisement to secure copulation and foraging of nuptial gifts. If these signals ease male mate searching, attractive male draglines are unnecessary. Overall, males may not invest in chemical stimulation but rather exploit female foraging interests through gift giving. Alternatively, they may release signals that prime other female sexual behaviours or towards which females may have evolved resistance.

Significance statement

Animals commonly use chemical signals to communicate during reproduction, and spiders have the potential to release such signals from their silk. We investigated whether two silk types, draglines released during movements and silk covering male nuptial gifts (prey offered to females at mating) are attractive to the opposite sex in a hunting spider. While males were attracted to female draglines, females did not respond to male silk of any type. Females may be using silk to advertise themselves to secure matings and food through reception of nuptial gifts. If males can successfully locate females, attracting females through draglines may be unnecessary. The finding that males do not release attractant signals in the silk cover of their nuptial gifts further suggests that rather than attempting to increase their attractiveness by using chemical stimulation, males may be uniquely exploiting females’ interest in food through gift giving behaviour.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Aisenberg A, Baruffaldi L, González M (2010) Behavioural evidence of male volatile pheromones in the sex-role reversed wolf spiders Allocosa brasiliensis and Allocosa alticeps. Naturwissenschaften 97(1):63–70. https://doi.org/10.1007/s00114-009-0612-z

    Article  PubMed  CAS  Google Scholar 

  2. Albo MJ, Costa-Schmidt LE, Costa FG (2009) To feed or to wrap? Female silk cues elicit male nuptial gift construction in a semiaquatic trechaleid spider. J Zool 277(4):284–290. https://doi.org/10.1111/j.1469-7998.2008.00539.x

    Article  Google Scholar 

  3. Albo MJ, Toft S, Bilde T (2011a) Condition dependence of male nuptial gift construction in the spider Pisaura mirabilis (Pisauridae). J Ethol 29(3):473–479. https://doi.org/10.1007/s10164-011-0281-1

    Article  Google Scholar 

  4. Albo MJ, Winther G, Tuni C, Toft S, Bilde T (2011b) Worthless donations: male deception and female counter play in a nuptial gift-giving spider. BMC Evol Biol 11(1):329. https://doi.org/10.1186/1471-2148-11-329

    Article  PubMed  PubMed Central  Google Scholar 

  5. Albo MJ, Toft S, Bilde T (2012) Female spiders ignore condition-dependent information from nuptial gift wrapping when choosing mates. Anim Behav 84(4):907–912. https://doi.org/10.1016/j.anbehav.2012.07.014

    Article  Google Scholar 

  6. Albo MJ, Toft S, Bilde T (2013) Sexual selection, ecology and evolution of nuptial gifts in spiders. Sex Sel Perspect Model Neotrop:183–200

  7. Amundsen T, Forsgren E (2001) Male mate choice selects for female coloration in a fish. Proc Natl Acad Sci 98(23):13155–13160. https://doi.org/10.1073/pnas.211439298

    Article  PubMed  CAS  Google Scholar 

  8. Andersen T, Bollerup K, Toft S, Bilde T (2008) Why do males of the spider Pisaura mirabilis wrap their nuptial gifts in silk: female preference or male control? Ethology 114(8):775–781. https://doi.org/10.1111/j.1439-0310.2008.01529.x

    Article  Google Scholar 

  9. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296–302

    Article  PubMed  Google Scholar 

  10. Arnqvist G, Rowe L (2013) Sexual conflict. Princeton University Press, Princeton

    Google Scholar 

  11. Baruffaldi L, Costa FG, Rodríguez A, González A (2010) Chemical communication in Schizocosa malitiosa: evidence of a female contact sex pheromone and persistence in the field. J Chem Ecol 36(7):759–767. https://doi.org/10.1007/s10886-010-9819-x

    Article  PubMed  CAS  Google Scholar 

  12. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823.

  13. Becker E, Riechert S, Singer F (2005) Male induction of female quiescence/catalepsis during courtship in the spider, Agelenopsis aperta. Behaviour 142(1):57–70. https://doi.org/10.1163/1568539053627767

    Article  Google Scholar 

  14. Bilde T, Tuni C, Elsayed R, Pekar S, Toft S (2007) Nuptial gifts of male spiders: sensory exploitation of the female’s maternal care instinct or foraging motivation? Anim Behav 73(2):267–273. https://doi.org/10.1016/j.anbehav.2006.05.014

    Article  Google Scholar 

  15. Bradbury JW, Vehrencamp SL (2011) Principles of animal communication, 2nd edn. Sinauer Associates, Inc., Massachussets

    Google Scholar 

  16. Bristowe WS, Locket GH (1926) The courtship of British lycosid spiders, and its probable significance. Proc Zool Soc 96(1):317–347. https://doi.org/10.1111/j.1096-3642.1926.tb01551.x

    Article  Google Scholar 

  17. Brum PED, Costa-Schmidt LE, De AAM (2012) It is a matter of taste: chemical signals mediate nuptial gift acceptance in a neotropical spider. Behav Ecol 23(2):442–447. https://doi.org/10.1093/beheco/arr209

    Article  Google Scholar 

  18. Cory A-L, Schneider JM (2016) Old maids have more appeal: effects of age and pheromone source on mate attraction in an orb-web spider. Peer J 4:e1877. https://doi.org/10.7717/peerj.1877

    Article  PubMed  CAS  Google Scholar 

  19. Cross FR, Jackson RR (2009) Mate-odour identification by both sexes of Evarcha culicivora, an East African jumping spider. Behav Process 81(1):74–79. https://doi.org/10.1016/j.beproc.2009.02.002

    Article  Google Scholar 

  20. Darwin C (1871) Sexual selection and the descent of man. Murray, London

    Google Scholar 

  21. Eisner T, Meinwald J (1995) The chemistry of sexual selection. Proc Natl Acad Sci 92(1):50–55. https://doi.org/10.1073/pnas.92.1.50

    Article  PubMed  CAS  Google Scholar 

  22. Fromhage L, Jennions M, Kokko H (2016) The evolution of sex roles in mate searching. Evolution (N Y) 70:617–624

    Google Scholar 

  23. Gaskett AC (2007) Spider sex pheromones: emission, reception, structures, and functions. 82:27–48

  24. Ghislandi PG, Albo MJ, Tuni C, Bilde T (2014) Evolution of deceit by worthless donations in a nuptial gift-giving spider. Curr Zool 60(1):43–51. https://doi.org/10.1093/czoolo/60.1.43

    Article  Google Scholar 

  25. Ghislandi PG, Beyer M, Velado P, Tuni C (2017) Silk wrapping of nuptial gifts aids cheating behaviour in male spiders. 28:744–749

  26. Havrilak JA, Shimmel KM, Rypstra AL, Persons MH (2014) Are you paying attention? Female wolf spiders increase dragline silk advertisements when males do not court. 345–352. doi: https://doi.org/10.1111/eth.12340

  27. Hegdekar BM, Dondale CD (1969) A contact sex pheromone and some response parameters in lycosid spiders. Can J Zool 47(1):1–4. https://doi.org/10.1139/z69-001

    Article  Google Scholar 

  28. Howard RW, Jackson LL, Banse H, Blows MW (2003) Cuticular hydrocarbons of Drosophila birchii and D. serrata: identification and role in mate choice in D. serrata. J Chem Ecol 29(4):961–976. https://doi.org/10.1023/A:1022992002239

    Article  PubMed  CAS  Google Scholar 

  29. Huber BA (2005) Sexual selection research on spiders: progress and biases. Biol Rev Camb Philos Soc 80(03):363–385. https://doi.org/10.1017/S1464793104006700

    Article  PubMed  Google Scholar 

  30. Johansson G, Jones M (2007) The role of chemical communication in mate choice. Biol Rev 82(2):265–289. https://doi.org/10.1111/j.1469-185X.2007.00009.x

    Article  PubMed  Google Scholar 

  31. Jones G, Barabas A, Elliott W, Parsons S (2002) Female greater wax moths reduce sexual display behavior in relation to the potential risk of predation by echolocating bats. Behav Ecol 13(3):375–380. https://doi.org/10.1093/beheco/13.3.375

    Article  Google Scholar 

  32. Kasumovic MM, Andrade MCB (2004) Discrimination of airborne pheromones by mate-searching male western black widow spiders (Latrodectus hesperus): species-and population-specific responses. Can J Zool 82(7):1027–1034. https://doi.org/10.1139/z04-081

    Article  Google Scholar 

  33. Kasumovic MM, Bruce MJ, Herberstein ME, Andrade MCB (2006) Risky mate search and mate preference in the golden orb-web spider (Nephila plumipes). Behav Ecol 18:189–195

    Article  Google Scholar 

  34. Lang A (1996) Silk investment in gifts by males of the nuptial feeding spider Pisaura mirabilis (Araneae: Pisauridae). Behaviour 133(9):697–716. https://doi.org/10.1163/156853996X00431

    Article  Google Scholar 

  35. McCartney J, Kokko H, Heller K-G, Gwynne DT (2012) The evolution of sex differences in mate searching when females benefit: new theory and a comparative test. Proc R Soc Lond B Biol Sci 279(1731):1225–1232. https://doi.org/10.1098/rspb.2011.1505

    Article  CAS  Google Scholar 

  36. Moore PJ, Reagan-Wallin NL, Haynes KF, Moore AJ (1997) Odour conveys status on cockroaches. Nature 389(6646):25. https://doi.org/10.1038/37888

    Article  CAS  Google Scholar 

  37. Nentwig W, Kuhn-Nentwig L (2013) Spider ecophysiology

  38. Nieberding CM, Fischer K, Saastamoinen M, Allen CE, Wallin EA, Hedenström E, Brakefield PM (2012) Cracking the olfactory code of a butterfly: the scent of ageing. Ecol Lett 15(5):415–424. https://doi.org/10.1111/j.1461-0248.2012.01748.x

    Article  PubMed  Google Scholar 

  39. Prokop P, Maxwell MR (2009) Female feeding and polyandry in the nuptially feeding nursery web spider, Pisaura mirabilis. Naturwissenschaften 96(2):259–265. https://doi.org/10.1007/s00114-008-0477-6

    Article  PubMed  CAS  Google Scholar 

  40. Prokop P, Maxwell MR (2012) Gift carrying in the spider Pisaura mirabilis: nuptial gift contents in nature and effects on male running speed and fighting success. Anim Behav 83(6):1395–1399. https://doi.org/10.1016/j.anbehav.2012.03.007

    Article  Google Scholar 

  41. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  42. Rantala MJ, Jokinen I, Kortet R, Vainikka A, Suhonen J (2002) Do pheromones reveal male immunocompetence? Proc R Soc Lond B Biol Sci 269(1501):1681–1685. https://doi.org/10.1098/rspb.2002.2056

    Article  Google Scholar 

  43. Rantala MJ, Kortet R, Kotiaho JS, Vainikka A, Suhonen J (2003) Condition dependence of pheromones and immune function in the grain beetle Tenebrio molitor. Funct Ecol 17(4):534–540. https://doi.org/10.1046/j.1365-2435.2003.00764.x

    Article  Google Scholar 

  44. Rhainds M (2010) Female mating failures in insects. Entomol Exp Appl 136(3):211–226. https://doi.org/10.1111/j.1570-7458.2010.01032.x

    Article  Google Scholar 

  45. Roberts JA, Uetz GW (2005) Information content of female chemical signals in the wolf spider, Schizocosa ocreata: male discrimination of reproductive state and receptivity. Anim Behav 70(1):217–223. https://doi.org/10.1016/j.anbehav.2004.09.026

    Article  Google Scholar 

  46. Roland C, Rovner JS (1983) Chemical and vibratory communication in the aquatic pisaurid spider Dolomedes triton. J Arachnol:77–85

  47. Rypstra AL, Wieg C, Walker SE, Persons MH (2003) Mutual mate assessment in wolf spiders: differences in the cues used by males and females. Ethology 109(4):315–325. https://doi.org/10.1046/j.1439-0310.2003.00874.x

    Article  Google Scholar 

  48. Rypstra AL, Schlosser AM, Sutton PL, Persons MH (2009) Multimodal signalling: the relative importance of chemical and visual cues from females to the behaviour of male wolf spiders (Lycosidae). Anim Behav 77(4):937–947. https://doi.org/10.1016/j.anbehav.2008.12.026

    Article  Google Scholar 

  49. Schulz S (2004) Semiochemistry of spiders. Adv Insect Chem Ecol 1:110–150

    Article  Google Scholar 

  50. Searcy LE, Rypstra AL, Persons MH (1999) Airborne chemical communication in the wolf spider Pardosa milvina. J Chem Ecol 25(11):2527–2533. https://doi.org/10.1023/A:1020878225553

    Article  CAS  Google Scholar 

  51. Shi PJ, Hu HSS, Xiao HJ (2013) Logistic regression is a better method of analysis than linear regression of arcsine square root transformed proportional diapause data of Pieris melete (Lepidoptera: Pieridae). Fla Entomol 96(3):1183–1185. https://doi.org/10.1653/024.096.0361

    Article  Google Scholar 

  52. Stålhandske P (2001) Nuptial gift in the spider Pisaura mirabilis maintained by sexual selection. Behav Ecol 12(6):691–697. https://doi.org/10.1093/beheco/12.6.691

    Article  Google Scholar 

  53. Stålhandske S (2002) Nuptial gifts of male spiders function as sensory traps. Proc R Soc Lond B Biol Sci 269(1494):905–908. https://doi.org/10.1098/rspb.2001.1917

    Article  Google Scholar 

  54. Stoltz JA, McNeil JN, Andrade MCB (2007) Males assess chemical signals to discriminate just-mated females from virgins in redback spiders. Anim Behav 74(6):1669–1674. https://doi.org/10.1016/j.anbehav.2007.03.011

    Article  Google Scholar 

  55. Taylor PW (1998) Dragline-mediated mate-searching in Trite planiceps (Araneae, Salticidae). J Arachnol:330–334

  56. Thomas ML (2011) Detection of female mating status using chemical signals and cues. Biol Rev 86(1):1–13.

    Article  PubMed  Google Scholar 

  57. Thomas ML, Simmons LW (2009) Sexual selection on cuticular hydrocarbons in the Australian field cricket, Teleogryllus oceanicus. BMC Evol Biol 9(1):162. https://doi.org/10.1186/1471-2148-9-162

    Article  PubMed  PubMed Central  Google Scholar 

  58. Toft S, Albo MJ (2015) Optimal numbers of matings: the conditional balance between benefits and costs of mating for females of a nuptial gift-giving spider. J Evol Biol 28(2):457–467. https://doi.org/10.1111/jeb.12581

    Article  PubMed  CAS  Google Scholar 

  59. Toft S, Albo MJ (2016) The shield effect: nuptial gifts protect males against pre-copulatory sexual cannibalism. Biol Lett 12(5):20151082. https://doi.org/10.1098/rsbl.2015.1082

    Article  PubMed  PubMed Central  Google Scholar 

  60. Tuni C, Berger-Tal R (2012) Male preference and female cues: males assess female sexual maturity and mating status in a web-building spider. Behav Ecol 23(3):582–587. https://doi.org/10.1093/beheco/ars001

    Article  Google Scholar 

  61. Tuni C, Bilde T (2010) No preference for novel mating partners in the polyandrous nuptial-feeding spider Pisaura mirabilis (Araneae: Pisauridae). Anim Behav 80(3):435–442. https://doi.org/10.1016/j.anbehav.2010.05.029

    Article  Google Scholar 

  62. Tuni C, Albo MJ, Bilde T (2013) Polyandrous females acquire indirect benefits in a nuptial feeding species. J Evol Biol 26(6):1307–1316. https://doi.org/10.1111/jeb.12137

    Article  PubMed  CAS  Google Scholar 

  63. Tuni C, Weber S, Bilde T, Uhl G (2017) Male spiders reduce pre-and postmating sexual investment in response to sperm competition risk. Behav Ecol 28(4):1030–1036. https://doi.org/10.1093/beheco/arx061

    Article  Google Scholar 

  64. Umbers KDL, Symonds MRE, Kokko H (2015) The mothematics of female pheromone signaling: strategies for aging virgins. Am Nat 185(3):417–432. https://doi.org/10.1086/679614

    Article  PubMed  Google Scholar 

  65. van Helsdingen PJ (1965) Sexual behaviour of Lepthyphantes leprosus (Ohlert) (Araneida, Linyphiidae), with notes on the function of the genital organs. Zool Meded 41:15–42

    Google Scholar 

  66. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313–320

    Article  Google Scholar 

  67. Wyatt TD (2003) Pheromones and animal behaviour communication by smell and taste. Cambridge University Press, Cambridge

    Google Scholar 

  68. Wyatt TD (2009) Fifty years of pheromones. Nature 457(7227):262–263. https://doi.org/10.1038/457262a

    Article  PubMed  CAS  Google Scholar 

  69. Xiao Y, Zhang J, Li S (2009) A two-component female-produced pheromone of the spider Pholcus beijingensis. J Chem Ecol 35(7):769–778. https://doi.org/10.1007/s10886-009-9660-2

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Patricia Velado Lobato for assistance in data collection and Federico Cappa for constructive contribution to the experimental design and comments on the manuscript.

Author information

Affiliations

Authors

Contributions

CT conceived the study, MB and TC designed the experiments, MB collected the data, TC analysed the data and CT led the writing of the manuscript with all authors contributing relevantly to the draft and giving final approval for publication.

Corresponding author

Correspondence to Cristina Tuni.

Additional information

Communicated by S. Sakaluk

Electronic supplementary material

ESM 1

(XLSX 28 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Beyer, M., Czaczkes, T.J. & Tuni, C. Does silk mediate chemical communication between the sexes in a nuptial feeding spider?. Behav Ecol Sociobiol 72, 49 (2018). https://doi.org/10.1007/s00265-018-2454-1

Download citation

Keywords

  • Silk
  • Sexual selection
  • Chemical signals
  • Nuptial gifts