Influence of past and current social contexts on hunting behaviour in spiderlings

Abstract

When foraging in a group, individuals adjust their behaviours to the actions of others in order to optimize their pay-offs. While many studies have examined the influence of group composition on behavioural strategies, relatively few have investigated how the presence or absence of conspecifics influences the expression of behaviours during hunting. Another aspect that has received little attention concerns the impact of prior social experience on the expression of predatory behaviour. Here, we studied how past and present social contexts influenced predatory behaviour in juveniles of the spider Agelena labyrinthica which, like most solitary species, exhibit a transient gregarious phase prior to dispersal. We tested, alone or in pairs, spiderlings that have been maintained in isolation or in groups for 24 h prior to behavioural assays. During the tests, we introduced a live prey to an experimental arena and we measured the latencies associated with the different phases of the hunting sequence. We found that spiders maintained in isolation captured prey faster than those kept in groups and that the presence of a sibling increased the latency of prey capture compared with individuals hunting alone. Such a social context effect adds another dimension to the already complex combination of factors that determine the success of spider foraging. Overall, our study reveals an influence of the social dimension, past and present, on hunting behaviour that may have been underestimated in carnivores.

Significance statement

It is generally considered that hunting in group increases individual benefits compared with solitary hunting. However, relatively few studies have compared hunting performance between individuals hunting alone or in group to assess how the presence of conspecifics impacts the expression of predatory behaviours. Another aspect that has been little explored concerns the role of the social context previously experienced on hunting behaviour. This study examined the influence of past or present social context on hunting behaviour in juveniles of a solitary spider during their gregarious phase. We showed that spiderlings maintained in isolation or tested alone were faster at catching prey than congeners reared socially or tested in groups. This study highlights a cost to sociality that has so far received little attention, and which could be an important element to consider in understanding transitions to permanent sociality.

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References

  1. Avilés L, Guevara J (2017) Sociality in spiders. In: Rubenstein D, Abbot P (Eds) Comparative Social Evolution. Cambridge, UK Cambridge Univ Press, pp 188–223

  2. Barth FG (1998) The vibrational sense of spiders. In: Comparative hearing: insects. Springer, pp 228–278

  3. Boesch C, Boesch H (1989) Hunting behavior of wild chimpanzees in the Taï National Park. Am J Phys Anthropol 78:547–573

    CAS  PubMed  Article  Google Scholar 

  4. Brosnan SF, Salwiczek L, Bshary R (2010) The interplay of cognition and cooperation. Philos Trans R Soc B Biol Sci 365:2699–2710

    Article  Google Scholar 

  5. Burgess JW (1976) Social spiders. Sci Am 234:100–107

    CAS  PubMed  Article  Google Scholar 

  6. Burgess JW (1979) Web-signal processing for tolerance and group predation in the social spider Mallos gregalis Simon. Anim Behav 27:157–164

    Article  Google Scholar 

  7. Chiara V, Ramon Portugal F, Jeanson R (2019) Social intolerance is a consequence, not a cause, of dispersal in spiders. PLoS Biol 17:e3000319

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. Chittka L, Skorupski P, Raine NE (2009) Speed-accuracy tradeoffs in animal decision making. Trends Ecol Evol 24:400–407

    PubMed  Article  Google Scholar 

  9. Dumke M, Herberstein ME, Schneider JM (2016) Producers and scroungers: feeding-type composition changes with group size in a socially foraging spider. Proc R Soc B Biol Sci 283:20160114

    Article  CAS  Google Scholar 

  10. Foelix R (2011) Biology of spiders. Oxford University Press USA

  11. Giraldeau L-A, Caraco T (2000) Social foraging theory. Princeton University Press

  12. Grinsted L, Bilde T, d'Ettorre P (2011) Cuticular hydrocarbons as potential kin recognition cues in a subsocial spider. Behav Ecol 22:1187–1194

    Article  Google Scholar 

  13. Grinsted L, Schou MF, Settepani V, Holm C, Bird TL, Bilde T (2020) Prey to predator body size ratio in the evolution of cooperative hunting—a social spider test case. Dev Genes Evol 230:173–184

    CAS  PubMed  Article  Google Scholar 

  14. Herberstein ME, Wignall AE, Hebets EA, Schneider JM (2014) Dangerous mating systems: signal complexity, signal content and neural capacity in spiders. Neurosci Biobehav Rev 46:509–518

    PubMed  Article  Google Scholar 

  15. Hvam A, Mayntz D, Nielsen RK (2005) Factors affecting cannibalism among newly hatched wolf spiders (Lycosidae, Pardosa amentata). J Arachnol 33:377–383

    Article  Google Scholar 

  16. Japyassú HF, Laland KN (2017) Extended spider cognition. Anim Cogn 20:375–395

    PubMed  PubMed Central  Article  Google Scholar 

  17. Kaston BJ (1965) Some little known aspects of spider behavior. Am Midl Nat 73:336–356

    Article  Google Scholar 

  18. Kim KW, Krafft B, Choe JC (2005) Cooperative prey capture by young subsocial spiders. Behav Ecol Sociobiol 59:92–100

    Article  Google Scholar 

  19. Krafft B, Cookson LJ (2012) The role of silk in the behaviour and sociality of spiders. Psyche A J Entomol 2012:529564

    Google Scholar 

  20. Krafft B, Pasquet A (1991) Synchronized and rhythmical activity during the prey capture in the social spider Anelosimus eximius (Araneae, Theridiidae). Insect Soc 38:83–90

    Article  Google Scholar 

  21. Kruuk H (1976) Feeding and social behaviour of the striped hyaena (Hyaena vulgaris Desmarest). Afr J Ecol 14:91–111

    Article  Google Scholar 

  22. Lesne P, Trabalon M, Jeanson R (2016) Cannibalism in spiderlings is not only about starvation. Behav Ecol Sociobiol 70:1669–1678

    Article  Google Scholar 

  23. Lubin Y, Bilde T (2007) The evolution of sociality in spiders. Adv Study Behav 37:83–145

    Article  Google Scholar 

  24. MacNulty DR, Tallian A, Stahler DR, Smith DW (2014) Influence of group size on the success of wolves hunting bison. PLoS One 9:e112884

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  25. Majer M, Svenning J-C, Bilde T (2015) Habitat productivity predicts the global distribution of social spiders. Front Ecol Evol 3

  26. Malli H, Kuhn-Nentwig L, Imboden H, Nentwig W (1999) Effects of size, motility and paralysation time of prey on the quantity of venom injected by the hunting spider Cupiennius salei. J Exp Biol 202:2083–2089

    CAS  PubMed  Google Scholar 

  27. Mayntz D, Toft S (2006) Nutritional value of cannibalism and the role of starvation and nutrient imbalance for cannibalistic tendencies in a generalist predator. J Anim Ecol 75:288–297

    PubMed  Article  Google Scholar 

  28. Morgenstern D, King GF (2013) The venom optimization hypothesis revisited. Toxicon 63:120–128

    CAS  PubMed  Article  Google Scholar 

  29. Mougenot F, Combe M, Jeanson R (2012) Ontogenesis and dynamics of aggregation in a solitary spider. Anim Behav 84:391–398

    Article  Google Scholar 

  30. Nisani Z, Dunbar SG, Hayes WK (2007) Cost of venom regeneration in Parabuthus transvaalicus (Arachnida: Buthidae). Comp Biochem Physiol Part A Mol Integr Physiol 147:509–513

    Article  CAS  Google Scholar 

  31. Packer C, Ruttan L (1988) The evolution of cooperative hunting. Am Nat 132:159–198

    Article  Google Scholar 

  32. Powers KS, Avilés L (2007) The role of prey size and abundance in the geographical distribution of spider sociality. J Anim Ecol 76:995–1003

    PubMed  Article  Google Scholar 

  33. Ruch J, Herberstein ME, Schneider JM (2014) Families hunt more successfully: effect of group composition on hunting and communal feeding. Anim Behav 91:171–178

    Article  Google Scholar 

  34. Schneider JM, Bilde T (2008) Benefits of cooperation with genetic kin in a subsocial spider. Proc Natl Acad Sci 105:10843–10846

    CAS  PubMed  Article  Google Scholar 

  35. Stander PE (1992) Cooperative hunting in lions: the role of the individual. Behav Ecol Sociobiol 29:445–454

    Article  Google Scholar 

  36. Szlep R (1964) Change in the response of spiders to repeated web vibrations. Behaviour 23:203–239

    Article  Google Scholar 

  37. Szymkowiak P (2014) Revision of Australian species of the genus Diaea (Araneae: Thomisidae) with redefinition of their taxonomic status. Annal Zool 64:333–477

    Article  Google Scholar 

  38. Trabalon M (2013) Chemical communication and contact cuticular compounds in spiders. In: Nentwig W (ed) Spider ecophysiology. Springer, Berlin, Heidelberg

    Google Scholar 

  39. Tretzel E (1961) Biologie, Ökologie und Brutpflege von Coelotes terrestris (Wider) (Araneae, Agelenidae). Z Morphol Oekol Tiere 50:375–542

    Article  Google Scholar 

  40. Vibert S, Scott C, Gries G (2014) A meal or a male: the ‘whispers’ of black widow males do not trigger a predatory response in females. Front Zool 11:4

    PubMed  PubMed Central  Article  Google Scholar 

  41. Ward PI, Enders MM (1985) Conflict and cooperation in the group feeding of the social spider Stegodyphus mimosarum. Behaviour 94:167–182

    Article  Google Scholar 

  42. Whitehousel ME, Lubin Y (2005) The functions of societies and the evolution of group living: spider societies as a test case. Biol Rev 80:347–361

    PubMed  Article  Google Scholar 

  43. Wignall AE, Herberstein ME (2013) Male courtship vibrations delay predatory behaviour in female spiders. Sci Rep 3:3557

    PubMed  PubMed Central  Article  Google Scholar 

  44. Wignall AE, Jackson RR, Wilcox RS, Taylor PW (2011) Exploitation of environmental noise by an araneophagic assassin bug. Anim Behav 82:1037–1042

  45. Wu C-H, Elias DO (2014) Vibratory noise in anthropogenic habitats and its effect on prey detection in a web-building spider. Anim Behav 90:47–56

    Article  Google Scholar 

  46. Yip EC, Rayor LS (2014) Maternal care and subsocial behaviour in spiders. Biol Rev 89:427–449

    PubMed  Article  Google Scholar 

  47. Yip EC, Powers KS, Avilés L (2008) Cooperative capture of large prey solves scaling challenge faced by spider societies. Proc Natl Acad Sci 105:11818–11822

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

We thank Simon Taquet for assistance in data collection and Iago Sanmartín Villar for insightful discussions. We are grateful to L Grinsted and one anonymous reviewer for their thoughtful comments on our manuscript.

Funding

VC was supported by a PhD grant from the French Ministry of Higher Education and Research. Funding was provided by CNRS (www.cnrs.fr) to RJ, Université Toulouse III (www.univ-tlse3.fr) to RJ and Ministère de la Recherche (www.enseignementsup-recherche.gouv.fr) to VC. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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VC: conceptualization, data curation, formal analysis, investigation, methodology, software, validation, visualization, writing—original draft, writing—review & editing. RJ: conceptualization, data curation, formal analysis, funding acquisition, investigation, methodology, project administration, resources, software, supervision, validation, visualization, writing—original draft, writing—review and editing.

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Correspondence to Violette Chiara.

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Chiara, V., Jeanson, R. Influence of past and current social contexts on hunting behaviour in spiderlings. Behav Ecol Sociobiol 74, 87 (2020). https://doi.org/10.1007/s00265-020-02870-9

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Keywords

  • Aggression
  • Communication
  • Foraging
  • Silk
  • Vibrational cues