Skip to main content
Log in

Copulatory behavior in a pholcid spider: males use specialized genitalic movements for sperm removal and copulatory courtship

  • Original Paper
  • Published:
Naturwissenschaften Aims and scope Submit manuscript

Abstract

Sexual selection may operate on pre-copulatory, copulatory, and post-copulatory traits. An example of a copulatory target of sexual selection is the genitalic movements a male performs during copulation. These movements may function either to prevent sperm competition or to influence a female’s fertilization decision. Here we investigated how copulation duration, pedipalp movements, and abdominal movements that males of the pholcid spider Holocnemus pluchei produce during copulation influence sperm removal and/or patterns of successful sperm transfer. We compared mating events with virgin and mated females for differences in copulatory and post-copulatory behavior. We expected longer copulation duration, longer pedipalp movement duration, and more complex and frequent pedipalp and abdominal movements when males mated with mated females compared to virgin females. Except for abdominal movements, our results corroborated these predictions. Furthermore, when we investigated mating events with mated females, we observed sperm mass ejection from the female gonopore and physical removal of sperm by males’ procursi. Females with interrupted second mating events showed a significant reduction of stored sperm masses compared to females with completed mating events. We suggest that males use alternating pedipalp movements to remove most of the rival sperm stored by mated females prior to sperm transfer. Copulation duration and pedipalp movements can be further used to transfer sperm and/or as a form of genitalic copulatory courtship.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Aisenberg A (2009) Male performance and body size affect female re-mating occurrence in the orb-web spider Leucauge mariana (Araneae, Tetragnathidae). Ethology 115:1127–1136

    Article  Google Scholar 

  • Aisenberg A, Costa FG (2005) Females mated without sperm transfer maintain high sexual receptivity in the wolf spider Schizocosa malitiosa. Ethology 111:545–558

    Article  Google Scholar 

  • Andrés J, Cordero Rivera A (2000) Copulation duration and fertilization success in a damselfly: an example of cryptic female choice? Anim Behav 59:695–703

    Article  PubMed  Google Scholar 

  • Austad SN (1984) Evolution of sperm priority patterns in spiders. In: Smith RL (ed) Sperm competition and the evolution of mating systems. Harvard University Press, Cambridge, pp 223–249

    Google Scholar 

  • Blumstein D T, Evans C S, Daniel J C (2000) JWatcher. http://galliform.psy. mq.edu.au/jwatcher/. Accessed 20 Nov 2008

  • Burger M (2007) Sperm dumping in a haplogyne spider. J Zool (Lond) 273:74–81

    Article  Google Scholar 

  • Calbacho-Rosa L, Córdoba-Aguilar A, Peretti A (2010) Occurrence and duration of post-copulatory mate guarding in a spider with last sperm precedence. Behaviour 147:1267–1283

    Article  Google Scholar 

  • Coddington JA, Levi HW (1991) Systematics and evolution of spiders (Araneae). Annu Rev Ecol Syst 22:565–592

    Google Scholar 

  • Córdoba-Aguilar A (1999) Male copulatory sensory stimulation induces female ejection of rival sperm in a damselfly. Proc R Soc Biol Sci Ser B 266:779–784

    Article  Google Scholar 

  • Córdoba-Aguilar A, Uhía E, Cordero Rivera A (2003) Sperm competition in Odonata (Insecta): the evolution of female sperm storage and rivals’ sperm displacement. J Zool (Lond) 261:381–398

    Article  Google Scholar 

  • Eberhard WG (1991) Copulatory courtship and cryptic female choice in insects. Biol Rev 66:1–31

    Article  Google Scholar 

  • Eberhard WG (1994) Evidence for widespread courtship during copulation in 131 species of insects and spiders, and implications for cryptic female choice. Evolution 48:711–733

    Article  Google Scholar 

  • Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton University Press, Princeton

    Google Scholar 

  • Eberhard WG (2001) The functional morphology of species-specific clasping structures on the front legs of male Archisepsis and Palaeosepsis flies (Diptera, Sepsidae). Zool J Linn Soc 133:335–368

    Article  Google Scholar 

  • Eberhard WG (2004) Why study spider sex: special traits of spiders facilitate studies of sperm competition and cryptic female choice. J Arachnol 32:545–556

    Article  Google Scholar 

  • Eberhard WG (2009) Postcopulatory sexual selection: Darwin’s omission and its consequences. Proc Natl Acad Sci USA 106:10025–10032

    Article  PubMed  CAS  Google Scholar 

  • Eberhard WG (2011) Experiments with genitalia: a commentary. Trends Ecol Evol 26:17–21

    Article  PubMed  Google Scholar 

  • Edvardsson M, Arnqvist G (2000) Copulatory courtship and cryptic female choice in red flour beetles Tribolium castaneum. Proc R Soc Biol Sci Ser B267:559–563

    Article  Google Scholar 

  • Elgar MA, Bathgate R (1996) Female receptivity and male mate-guarding in the jewel spider Gasteracantha minax Thorell (Araneidae). J Insect Behav 9:729–738

    Article  Google Scholar 

  • Foelix RF (1982) The biology of spiders. Harvard University Press, Cambridge

    Google Scholar 

  • Herbestein ME (2011) Spider behaviour: flexibility and versatility. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Huber BA (1995) Copulatory mechanism in Holocnemus pluchei and Pholcus opilionoides, with notes on male cheliceral apophyses and stridulatory organs in Pholcidae (Araneae). Acta Zool (Stockh) 76:291–300

    Article  Google Scholar 

  • Huber BA (1998) Genital mechanics in some neotropical pholcid spiders (Araneae: Pholcidae) with implications for systematics. J Zool (Lond) 244:587–599

    Article  Google Scholar 

  • Huber BA (2005) Sexual selection research on spiders: progress and biases. Biol Rev 80:363–385

    Article  PubMed  Google Scholar 

  • Huber BA, Eberhard WG (1997) Courtship, copulation, and genital mechanics in Physocyclus globosus (Araneae, Pholcidae). Can J Zool 74:905–918

    Article  Google Scholar 

  • Jakob EM (1991) Costs and benefits of group living for pholcid spiderlings: losing food, saving silk. Anim Behav 41:711–722

    Article  Google Scholar 

  • Kaster JL, Jakob EM (1997) Last-male sperm priority in a haplogyne spider (Araneae: Pholcidae): correlations between female morphology and patterns of sperm usage. Ann Entomol Soc Am 90:254–259

    Google Scholar 

  • Kelly CD, Jennions MD (2011) Sexual selection and sperm quantity: meta-analyses of strategic ejaculation. Biol Rev 86:863–884

    Article  PubMed  Google Scholar 

  • Leonard J, Córdoba-Aguilar A (eds) (2010) The evolution of primary characters in animals. Oxford University Press, Oxford

    Google Scholar 

  • Marcotte M, Delisle J, McNeil JN (2005) Impact of male mating history on the temporal sperm dynamics of Choristoneura rosaceana and C. fumiferana females. J Insect Physiol 51:537–544

    Article  PubMed  CAS  Google Scholar 

  • Michiels NK (1989) Morphology of male and female genitalia in Sympetrum danae (Sulzer), with special reference to the mechanism of sperm removal during copulation (Anisoptera: Libellulidae). Odonatologica 18:21–31

    Google Scholar 

  • Naud MJ, Hanlon RT, Hall KC, Shaw PW, Havenhand JN (2004) Behavioural and genetic assessment of reproductive success in a spawning aggregation of the Australian giant cuttlefish, Sepia apama. Anim Behav 67:1043–1050

    Article  Google Scholar 

  • Ono T, Siva-Jothy MT, Kato A (1989) Removal and subsequent ingestion of rivals’ semen during copulation in a tree cricket. Physiol Entomol 14:195–202

    Article  Google Scholar 

  • Otronen M (1990) Mating behavior and sperm competition in the fly, Dryomyza anilis. Behav Ecol Sociobiol 26:349–356

    Article  Google Scholar 

  • Otronen M, Siva-Jothy MT (1991) The effect of postcopulatory male-behavior on ejaculate distribution within the female sperm storage organs of the fly, Dryomyza anilis (Diptera, Dryomyzidae). Behav Ecol Sociobiol 29:33–37

    Article  Google Scholar 

  • Parker GA (1979) Sexual selection and sexual conflict. In: Blum MS, Blum NA (eds) Sexual selection and reproductive competition in insects. Academic Press, New York, pp 123–166

    Google Scholar 

  • Peretti AV, Eberhard WG (2010) Cryptic female choice via sperm dumping favours male copulatory courtship in a spider. J Evol Biol 23:271–281

    Article  PubMed  CAS  Google Scholar 

  • Peretti AV, Eberhard W, Briceño D (2006) Copulatory dialogue: female spiders sing during copulation to influence male genitalic movements. Anim Behav 72:413–421

    Article  Google Scholar 

  • Pilastro A, Scaggiante M, Rasotto MB (2002) Individual adjustment of sperm expenditure accords with sperm competition theory. Proc Natl Acad Sci U S A 99:9913–9915

    Article  PubMed  CAS  Google Scholar 

  • Pizzari T, Birkhead T (2000) Female feral fowl eject sperm of subdominant males. Nature 405:787–789

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez V, Windsor D, Eberhard WG (2004) Tortoise beetle genitalia and demonstration of a sexually selected advantage for flagellum length in Chelymorpha alternans (Chrysomelidae, Cassidini, Stolaini). In: Jolivet P, Santiago-Blay JA, Schmitt M (eds) New developments in the biology of Chrysomelidae. Academic Publishing, The Hague, SPB, pp 739–748

    Google Scholar 

  • Schäfer MA, Uhl G (2002) Determinants of paternity success in the Pholcus phalangioides (Pholcidae, Araneae): the role of male and female mating behaviour. Behav Ecol Sociobiol 51:368–377

    Article  Google Scholar 

  • Schäfer MA, Misof B, Uhl G (2008) Effects of body size of both sexes and female mating history on male behaviour and paternity success in a spider. Anim Behav 76:75–86

    Article  Google Scholar 

  • Simmons LW (2001) Sperm competition and its evolutionary consequences in the insects. Princeton University Press, Princeton, New Jersey

    Google Scholar 

  • Snook RR, Hosken DJ (2004) Sperm death and dumping in Drosophila. Nature 428:939–941

    Article  PubMed  CAS  Google Scholar 

  • Solensky MJ, Oberhauser KS (2009) Male monarch butterflies, Danaus plexippus, adjust ejaculates in response to intensity of sperm competition. Anim Behav 77:465–472

    Article  Google Scholar 

  • Uhl G (1994) Genital morphology and sperm storage in Pholcus phalangioides (Fuesslin, 1775) (Pholcidae: Araneae). Acta Zool (Stockh) 75:1–12

    Article  Google Scholar 

  • von Helversen D, von Helversen O (1991) Pre-mating sperm removal in the bush cricket Metaplastes Ramme 1931 (Orthoptera, Tettigonoidea, Phaneropteridae). Behav Ecol Sociobiol 28:391–396

    Article  Google Scholar 

  • Waage JK (1979) Dual function of the damselfly penis: sperm removal and sperm transfer. Science 203:916–918

    Article  PubMed  CAS  Google Scholar 

  • Wada T, Takegaki T, Mori T, Natsukari Y (2006) Reproductive behavior of the Japanese spineless cuttlefish Sepiella japonica. Venus 65:221–228

    Google Scholar 

  • Wada T, Takegaki T, Mori T, Natsukari Y (2010) Sperm removal, ejaculation and their behavioral interaction in male cuttlefish in response to female mating history. Anim Behav 79:613–619

    Article  Google Scholar 

Download references

Acknowledgments

We thank Margarita Chiaraviglio and Cristina Sciocia for suggestions on the manuscript. The authors also acknowledge D. Vrech and P. Olivero for help during collecting and rearing. Financial support was provided by the Consejo Nacional de Investigaciones Científicas y Técnicas, FONCYT, and Secretaria de ciencia y técnica–Universidad Nacional de Córdoba of Argentina and Agencia Nacional de Investigación, España. Four reviewers and Chris Anderson provided highly useful comments to previous versions.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Lucía Calbacho-Rosa or Alex Córdoba-Aguilar.

Additional information

Communicated by: Sven Thatje

Electronic supplementary material

Below is the link to the electronic supplementary material.

Male carrying out alternating pedipalp movements, overview (MPG 3214 kb)

Male carrying out alternating pedipalp movements, detailed view (MPG 1720 kb)

Male carrying out simultaneous pedipalp movements (MPG 4272 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Calbacho-Rosa, L., Galicia-Mendoza, I., Dutto, M.S. et al. Copulatory behavior in a pholcid spider: males use specialized genitalic movements for sperm removal and copulatory courtship. Naturwissenschaften 100, 407–416 (2013). https://doi.org/10.1007/s00114-013-1038-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00114-013-1038-1

Keywords

Navigation