Elsevier

Animal Behaviour

Volume 168, October 2020, Pages 59-68
Animal Behaviour

Biting and binding: an exclusive coercive mating strategy of males in a philodromid spider

https://doi.org/10.1016/j.anbehav.2020.08.001Get rights and content

Highlights

  • Males of the spider T. fabricii bite females instead of courting.

  • Females are inseminated by males after being immobilized by male bites.

  • Males also bind females with silk to prolong the state of immobility.

  • After the copulation females are less mobile than they were before.

  • Larger venom glands of males indicate their adaptation to coerce females to mate.

Males typically court females extensively to convince them to mate. In some species, however, males coerce females to mate. We studied mating behaviour in the spider Thanatus fabricii and focused on behavioural and venomic adaptations. We found that males always bit and bound females before and during mating. The bitten females quickly fell into a state of immobility, during which males copulated with them. The duration of male bites increased with increasing size of the female. In contrast, male bites were shorter if the female was missing legs. Additionally, males with relatively longer legs induced longer states of immobility in females. Binding by silk prolonged the state of immobilization, allowing males to perform more insertions. After copulation, females were less successful in catching their prey (ants), suggesting that this mating strategy negatively affects female fitness. Altogether, this evidence shows that mating in T. fabricii is coercive. Males of T. fabricii had relatively larger venom glands than both conspecific females and males of closely related Philodromus species, which court females. The composition of venom, however, did not differ between the sexes. Male venom glands appear to be adapted to coercive mating rather than to foraging, as they caught fewer prey than closely related species. We suggest that coercive mating in T. fabricii may be enabled by venomic adaptation in the males.

Section snippets

Mating and Its Effect on the Female

Adult and subadult males and females of T. fabricii were hand-collected from the ground around Dimona, Israel, on 1 day in April 2019. The spiders were housed individually in plastic vials and kept at room temperature (approximately 22 °C) and under a natural light:dark regime. To maintain humidity, the spiders in vials were kept in plastic bags in which a tissue was placed and moistened every 3 days with a few drops of water. The spiders were fed with three fruit flies, Drosophila melanogaster,

Mating Sequence

During mating, a male approached a female quickly from one side or from behind (see Video S1 in the Supplementary Material). The female tried to flee from the male, which resulted in a struggle when the male attempted to grab her appendage and bite it. The bites were followed by a state of immobility: the female drew her legs up close to her body and became completely inactive and immobile. Then the male mounted her and laid silk on her legs and body. During silk laying, the male tapped the

Discussion

We found that, instead of courting, males of the spider T. fabricii attacked and bit their mates. The females, in turn, became immobile and, in this state, were inseminated by the males. Several behavioural features indicate that mating in this species is coercive and that this strategy might be harmful to females: (1) males used fast movements, biting and silk laying to restrain the female; (2) females showed deterrent behaviours to male mating attempts; (3) males injured females during

Acknowledgments

We thank Yael Lubin for facilitating the collection of T. fabricii and Messor ant workers in Israel. We are also grateful to Stanislav Korenko, who helped with the collection, and to Ondřej Machač, who informed us about behaviour resembling coercive mating in another Thanatus species. We are indebted to Martina Hrušková-Martišová who gave valuable comments on the manuscript. This work was supported by MEYS CR via the CIISB research infrastructure project LM2018127 which enabled us to conduct

References (62)

  • A. Aisenberg et al.

    Silk release by copulating Schizocosa malitiosa males (Araneae, Lycosidae): A bridal veil

    Journal of Arachnology

    (2008)
  • M.J. Albo et al.

    Condition dependence of male nuptial gift construction in the spider Pisaura mirabilis (Pisauridae)

    Journal of Ethology

    (2011)
  • A.G. Anderson et al.

    Benefits of size dimorphism and copulatory silk wrapping in the sexually cannibalistic nursery web spider, Pisaurina mira

    Biological Letters

    (2016)
  • M. Andersson

    Sexual selection

    (1994)
  • G. Arnqvist et al.

    Sexual conflict

    (2005)
  • Y.G. Baba et al.

    Dead or alive? Sexual conflict and lethal copulatory interactions in long-jawed Tetragnatha spiders

    Behavioral Ecology

    (2018)
  • L. Baruffaldi et al.

    Neutral fitness outcomes contradict inferences of sexual ‘coercion’ derived from male's damaging mating tactic in a widow spider

    Scientific Reports

    (2017)
  • E. Becker et al.

    Male induction of female quiescence/catalepsis during courtship in the spider, Agelenopsis aperta

    Behaviour

    (2005)
  • A. Bisazza et al.

    Female mate choice in a mating system dominated by male sexual coercion

    Behavioral Ecology

    (2001)
  • M.E. Braunwalder

    Fauna Helvetica 13: Scorpiones (Arachnida)

    (2005)
  • W.S. Bristowe

    XIII.—the mating habits of British Thomisid and Sparassid spiders

    Annals and Magazine of Natural History

    (1926)
  • W.S. Bristowe

    The mating habits of spiders: A second supplement, with the description of a new thomisid from Kratkatau

    Proceedings of the Zoological Society of London

    (1931)
  • W.D. Brown et al.

    Sexual conflict and the evolution of mating systems

  • M.A. Elgar

    Sexual cannibalism in spiders and other invertebrates

  • R. Foelix

    Biology of spiders

    (2011)
  • O.F. Francke

    Observations on the reproductive biology and life history of Megacormus gertschi Diaz (Scorpiones: Chactidae; Megacorminae)

    Journal of Arachnology

    (1979)
  • L. Fromhage et al.

    Safer sex with feeding females: Sexual conflict in a cannibalistic spider

    Behavioral Ecology

    (2004)
  • A.C. Gaskett

    Spider sex pheromones: Emission, reception, structures, and functions

    Biological Reviews

    (2007)
  • K.N. Gibson et al.

    Intra-community infanticide and forced copulation in spider monkeys: A multi-site comparison between Cocha Cashu, Peru and Punta Laguna, Mexico

    American Journal of Primatology

    (2008)
  • M. Gregorič et al.

    Spider behaviors include oral sexual encounters

    Scientific Reports

    (2016)
  • O. von Helversen

    Gedanken zur Evolution der Paarungsstellung bei den Spinnen (Arachnida: Araneae)

    Entomologica Germanica

    (1976)
  • Cited by (6)

    • Waking beauties: Mating quiescence in arachnid females

      2023, Advances in the Study of Behavior
    • Fertility signalling games: should males obey the signal?

      2023, Philosophical Transactions of the Royal Society B: Biological Sciences
    View full text