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Stridulation can suppress cannibalism in a specialised araneophagous predator

  • Eva Líznarová
  • Lenka Sentenská
  • František Šťáhlavský
  • Stano Pekár
Original Article

Abstract

Acoustic signalling is widespread in arthropods and appears to be common in spiders, but the function is still unknown in many species. Acoustic signals have several functions and can be used both in interspecific (e.g., to threaten potential predators) and intraspecific (during courtship) communication. In our study, we investigated the intraspecific role of stridulation in the araneophagous Palpimanus spider (Araneae: Palpimanidae). These spiders are specialised in hunting other spiders at all ontogenetic stages. We hypothesised that stridulation is used to avoid cannibalism. We investigated the morphology of the stridulatory apparatus, analysed the acoustic signals that various stages produce, and found two types of stridulation, low- and high-intensity stridulation. Then, we investigated the presence of cannibalism between individuals of variable body size and the use of stridulation during interactions. We found that cannibalism occurred only when the prosoma size difference between the two opponents was more than 200%. Then, we paired conspecific large control Palpimanus with smaller control individual or with individual whose stridulatory organs were impaired and found that impaired spiders suffered significantly higher cannibalism than the control spiders. Our study reveals a novel role of acoustic communication in the conspecific recognition of araneophagous spiders.

Significance statement

Cannibalism is widespread among predatory animals. However, cannibalism might not be an optimal strategy for several reasons and should be a less preferred option for predators. Palpimanus spiders are prey specialised predators preying primarily on other spiders thus the risk of cannibalism is even higher than in generalist predators. These spiders possess stridulatory apparatus and they often stridulate following a contact with conspecifics. We found that cannibalism occasionally occurred during contact with conspecifics and that the probability of cannibalism increased with the size difference between the interacting individuals. When the spiders were not able to stridulate during contact, the probability of cannibalism increased significantly. Our results thus show that Palpimanus spiders use stridulation to reduce cannibalism among unequally sized individuals.

Keywords

Acoustic signal Araneophagy Defence Intraspecific interaction Predation Spider 

Notes

Acknowledgments

We would like to thank Ladislav Ilkovics from the Department of Histology and Embryology at the Medical Faculty of Masaryk University, for help in taking SEM pictures. We thank Stanislav Korenko for help in collecting spider specimens. We also thank to three anonymous reviewers for their comments.

Authors’ contributions

SP conceived the study, acquired and analyse data on morphology and stridulation and conducted comparative analysis; EL acquired and analyse behavioural data; LS acquired behavioural data; EL, LS, SP and FŠ collected tested specimens. EL and SP interpreted data and wrote the manuscript. LS and FŠ helped to draft the manuscript. All the authors gave final approval for publication.

Compliance with ethical standards

Data availability statement

The datasets generated and analysed during the current study are available in the Terrestrial invertebrate research group repository, http://www.sci.muni.cz/zoolecol/inverteb/?page_id=18.

Supplementary material

265_2018_2541_MOESM1_ESM.mp4 (4.2 mb)
ESM 1 (MP4 4329 kb)

References

  1. Alexander AJ (1958) On the stridulation of scorpions. Behaviour 12:339–352CrossRefGoogle Scholar
  2. Alexander AJ (1960) A note on the evolution of stridulation within the family Scorpionidae. Proc Zool Soc London 133:391–399CrossRefGoogle Scholar
  3. Alexander RD (1967) Acoustical communication in arthropods. Annu Rev Entomol 12:495–526CrossRefGoogle Scholar
  4. Barth FG, Schmitt A (1991) Species recognition and species isolation in wandering spiders (Cupiennius spp.; Ctenidae). Behav Ecol Sociobiol 29:333–339CrossRefGoogle Scholar
  5. Belles-Isles JC, Fitzgerald GJ (1993) A fitness advantage of cannibalism in female sticklebacks (Gasterosteus aculeatus L.). Ethol Ecol Evol 5:187–191CrossRefGoogle Scholar
  6. Bouwma PE, Herrnkind WF (2009) Sound production in Caribbean spiny lobster Panulirus argus and its role in escape during predatory attack by Octopus briareus. N Z J Mar Freshw Res 43:3–13CrossRefGoogle Scholar
  7. Broughton WB (1963) Method in bio-acoustic terminology. In: Busnel RG (ed) Acoustic behaviour of animals. Elsevier, Amsterdam, pp 3–47Google Scholar
  8. Cerveira AM, Jackson RR (2005) Specialised predation by Palpimanus sp. (Araneae: Palpimanidae) on jumping spiders (Araneae: Salticidae). J East Afr Nat Hist 94:303–317CrossRefGoogle Scholar
  9. Claridge M (2006) Insect sounds and communication—an introduction. In: Drosopoulos S, Claridge MF (eds) Insect Sounds and Communication. Physiology, Behaviour, Ecology and Evolution. CRC Press, Boca Raton, pp 3–10Google Scholar
  10. Cloudsley-Thompson JL, Constantinou C (1984) Stridulatory apparatus of Solifugae (Solpugida). J Arid Environ 7:365–369Google Scholar
  11. Dumortier B (1963) Morphology of sound emission apparatus in Arthropoda. In: Busnel RG (ed) Acoustic behaviour of animals. Elsevier Pub. Co., Amsterdam, pp 277–345Google Scholar
  12. Dutto MS, Calbacho-Rosa L, Peretti AV (2011) Signaling and sexual conflict: female spiders use stridulation to inform males of sexual receptivity. Ethology 117:1040–1049CrossRefGoogle Scholar
  13. Elgar MA (1992) Sexual cannibalism in spiders and other invertebrates. In: Elgar MA, Crespi BJ (eds) Cannibalism: ecology and evolution among diverse taxa. Oxford University Press, Oxford, pp 129–156Google Scholar
  14. Elias DO, Hebets EA, Hoy RR, Mason AC (2005) Seismic signals are crucial for male mating success in a visual specialist jumping spider (Araneae: Salticidae). Anim Behav 69:931–938CrossRefGoogle Scholar
  15. Elias DO, Kasumovic MM, Punzalan D, Andrade MC, Mason AC (2008) Assessment during aggressive contests between male jumping spiders. Anim Behav 76:901–910CrossRefPubMedPubMedCentralGoogle Scholar
  16. Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Evol Syst 6:87–106CrossRefGoogle Scholar
  17. Gibson JS, Uetz GW (2008) Seismic communication and mate choice in wolf spiders: components of male seismic signals and mating success. Anim Behav 75:1253–1262CrossRefGoogle Scholar
  18. Guarisco H (1988) Predation of Achaearanea tepidariorum (Araneae, Theridiidae) upon Sphodros fitchi (Araneae, Atypidae). J Arachnol 16:390–391Google Scholar
  19. Guseinov EFO (2006) The prey of a lithophilous crab spider Xysticus loeffleri (Araneae, Thomisidae). J Arachnol 34:37–45CrossRefGoogle Scholar
  20. Gwynne DT, Dadour IR (1985) A new mechanism of sound production by courting male jumping spiders (Araneae: Salticidae, Saitis michaelseni Simon). J Zool 207:35–42CrossRefGoogle Scholar
  21. Henschel JR, Lubin YD (1997) A test of habitat selection at two spatial scales in a sit-and-wait predator: a web spider in the Namib dunes. J Anim Ecol 66:401–413CrossRefGoogle Scholar
  22. Heuts BA, Brunt T (2001) Transitive predatory relationships of spider species (Arachnida, Araneae) in laboratory tests. Behav Process 53:57–64CrossRefGoogle Scholar
  23. Hill SA (2007) Sound generation in Mantis religiosa (Mantodea: Mantidae): stridulatory structures and acoustic signal. J Orthoptera Res 16:35–49CrossRefGoogle Scholar
  24. Hinton HE, Wilson RS (1970) Stridulatory organs in spiny orb-weaver spiders. J Zool 162:481–484CrossRefGoogle Scholar
  25. Hrušková-Martišová M, Pekár S, Gromov A (2008) Analysis of the stridulation in solifuges (Arachnida: Solifugae). J Insect Behav 21:440–449CrossRefGoogle Scholar
  26. Huber BA, Eberhard WG (1997) Courtship, copulation, and genital mechanics in Physocyclus globosus (Araneae, Pholcidae). Can J Zool 75:905–918CrossRefGoogle Scholar
  27. Iida H (2003) Small within-clutch variance in spiderling body size as a mechanism for avoiding sibling cannibalism in the wolf spider Pardosa pseudoannulata (Araneae: Lycosidae). Popul Ecol 45:1–6Google Scholar
  28. Jackson RR (1992) Eight-legged tricksters: spiders that specialize at catching other spiders. Bioscience 42:590–598CrossRefGoogle Scholar
  29. Jackson RR, Li D, Fijn N, Barrion AT (1998) Predator-prey interactions between aggressive-mimic jumping spiders (Salticidae) and araneophagic spitting spiders (Scytodidae) from the Philippines. J Insect Behav 11:319–342CrossRefGoogle Scholar
  30. Jocqué R (2005) Six stridulating organs on one spider (Araneae, Zodariidae): is this the limit? J Arachnol 33:597–603CrossRefGoogle Scholar
  31. Johansson F (1996) The influence of cannibalism and prey density on growth in the damselfly Coenagrion hastulatum. Arch Hydrobiol 137:523–535Google Scholar
  32. Jones G (2005) Echolocation. Curr Biol 15:R484–R488CrossRefPubMedGoogle Scholar
  33. Kirchner WH, Röschard J (1999) Hissing in bumblebees: an interspecific defence signal. Insect Soc 46:239–243CrossRefGoogle Scholar
  34. Land MF (1985) The morphology and optics of spider eyes. In: Barth FG (ed) Neurobiology of arachnids. Springer-Verlag, Berlin, pp 53–78CrossRefGoogle Scholar
  35. Land MF, Nilsson DE (2012) Animal eyes. Oxford University Press, OxfordCrossRefGoogle Scholar
  36. Lazzari CR, Manrique G, Schilman PE (2006) Vibratory communication in Triatominae (Heteroptera). In: Drosopoulos S, Claridge MF (eds) Insect sounds and communication: physiology, behaviour, ecology and evolution. CRC Press, Boca Raton, pp 297–304Google Scholar
  37. Lee RCP, Nyffeler M, Krelina E, Pennycook BW (1986) Acoustic communication in two spider species of the genus Steatoda (Araneae, Theridiidae). Mitt Schweiz Entomol Ges 59:337–348Google Scholar
  38. Legendre R (1963) L'audition et l'émission de sons chez les aranéides. Ann Biol 11:371–390Google Scholar
  39. Legendre R (1970) Arachnides-Araignées-Archaeidae. Faune Madag 32:1–51Google Scholar
  40. Li D, Jackson RR (1996a) Prey-specific capture behaviour and prey preferences of myrmecophagic and araneophagic jumping spiders (Araneae: Salticidae). Rev Suisse Zool:423–436Google Scholar
  41. Li D, Jackson RR (1996b) How temperature affects development and reproduction in spiders: a review. J Therm Biol 21:245–274CrossRefGoogle Scholar
  42. Lourenço WR, Cloudsley-Thompson JL (1995) Stridulatory apparatus and the evolutionary significance of sound production in Rhopalurus species (Scorpiones: Buthidae). J Arid Environ 31:423–429CrossRefGoogle Scholar
  43. MacNeil C, Dick JTA, Hatcher MJ, Fielding NJ, Hume KD, Dunn AM (2003) Parasite transmission and cannibalism in an amphipod (Crustacea). Int J Parasitol 33:795–798CrossRefPubMedGoogle Scholar
  44. Maddison WP, Stratton GE (1988) Sound production and associated morphology in male jumping spiders of the Habronattus agilis species group (Araneae, Salticidae). J Arachnol 16:199–211Google Scholar
  45. Manrique G, Schilman PE (2000) Two different vibratory signals in Rhodnius prolixus (Hemiptera: Reduviidae). Acta Trop 77:271–278CrossRefPubMedGoogle Scholar
  46. Marshall SD, Thoms EM, Uetz GW (1995) Setal entanglement: an undescribed method of stridulation by a neotropical tarantula (Araneae: Theraphosidae). J Zool 235:587–595CrossRefGoogle Scholar
  47. Masters WM (1979) Insect disturbance stridulation: its defensive role. Behav Ecol Sociobiol 5:187–200CrossRefGoogle Scholar
  48. Oelbermann K, Scheu S (2002) Effects of prey type and mixed diets on survival, growth and development of a generalist predator, Pardosa lugubris (Araneae: Lycosidae). Basic Appl Ecol 3:285–291CrossRefGoogle Scholar
  49. Pekár S, Brabec M (2016) Marginal models via GLS: a convenient yet neglected tool for analysis of correlated data in behavioural sciences. Ethology 122:621–631CrossRefGoogle Scholar
  50. Pekár S, Brabec M (2018) Marginal models via GEE: a convenient yet neglected tool for analysis of correlated data in behavioural sciences. Ethology 124:86–93CrossRefGoogle Scholar
  51. Pekár S, Šobotník J, Lubin Y (2011) Armoured spiderman: morphological and behavioural adaptations of a specialised araneophagous predator (Araneae: Palpimanidae). Naturwissenschaften 98:593–603CrossRefPubMedGoogle Scholar
  52. Peretti A, Eberhard WG, Briceño RD (2006) Copulatory dialogue: female spiders sing during copulation to influence male genitalic movements. Anim Behav 72:413–421CrossRefGoogle Scholar
  53. Pérez-Miles F, Oca LMD, Postiglioni R, Costa FG (2005) The stridulatory setae of Acanthoscurria suina (Araneae, Theraphosidae) and their possible role in sexual communication: an experimental approach. Iheringia, Sér Zool 95:365–371CrossRefGoogle Scholar
  54. Pfennig DW, Reeve HK, Sherman PW (1993) Kin recognition and cannibalism in spadefoot toad tadpoles. Anim Behav 46:87–94CrossRefGoogle Scholar
  55. Pfennig DW, Ho SG, Hoffman EA (1998) Pathogen transmission as a selective force against cannibalism. Anim Behav 55:1255–1261CrossRefPubMedGoogle Scholar
  56. Pinheiro JC, Bates DM (2000) Linear mixed-effects models: basic concepts and examples. Mixed-effects models in S and S-plus. Springer-Verlag, New YorkGoogle Scholar
  57. Pizzatto L, Shine R (2011) You are what you eat: parasite transfer in cannibalistic cane toads. Herpetologica 67:118–123CrossRefGoogle Scholar
  58. Platnick NI (1981) A review of the spider subfamily Palpimaninae (Araneae, Palpimanidae). Bull Br Arachnol Soc 5:169–173Google Scholar
  59. Pocock RI (1895) Musical boxes in spiders. Nat Sci 6:44–50Google Scholar
  60. Polidori C, Pavan G, Ruffato G, Asís JD, Tormos J (2013) Common features and species-specific differences in stridulatory organs and stridulation patterns of velvet ants (Hymenoptera: Mutillidae). Zool Anz Comp Zool 252:457–468CrossRefGoogle Scholar
  61. Pomini AM, Machado G, Pinto-da-Rocha R, Macías-Ordóñez R, Marsaioli AJ (2010) Lines of defense in the harvestman Hoplobunus mexicanus (Arachnida: Opiliones): aposematism, stridulation, thanatosis, and irritant chemicals. Biochem Syst Ecol 38:300–308CrossRefGoogle Scholar
  62. R Development Core Team (2015) R: a language and environment for statistical computing. In: R foundation for statistical computing. Vienna, AustriaGoogle Scholar
  63. Riechert SE (1978) Games spiders play: behavioral variability in territorial disputes. Behav Ecol Sociobiol 3:135–162CrossRefGoogle Scholar
  64. Samu F, Toft S, Kiss B (1999) Factors influencing cannibalism in the wolf spider Pardosa agrestis (Araneae, Lycosidae). Behav Ecol Sociobiol 45:349–354CrossRefGoogle Scholar
  65. Schilman PE, Lazzari CR, Manriqueb G (2001) Comparison of disturbance stridulations in five species of triatominae bugs. Acta Trop 79:171–178CrossRefPubMedGoogle Scholar
  66. Schmidt JM (1994) Encounters between adult spined assassin bugs, Sinea diadema (F.)(Hemiptera: Reduviidae): the occurrence and consequences of stridulation. J Insect Behav 7:811–828CrossRefGoogle Scholar
  67. Schmidt JO, Blum MS (1977) Adaptations and responses of Dasymutilla occidentalis (Hymenoptera: Mutillidae) to predators. Entomol Exp Appl 21:99–111CrossRefGoogle Scholar
  68. Schmitt A, Schuster M, Barth FG (1992) Male competition in a wandering spider (Cupiennius getazi, Ctenidae). Ethology 90:293–306CrossRefGoogle Scholar
  69. Sentenská L, Pekár S (2014) Eat or not to eat: reversed sexual cannibalism as a male foraging strategy in the spider Micaria sociabilis (Araneae: Gnaphosidae). Ethology 120:511–518CrossRefGoogle Scholar
  70. Shear WA (1970) Stridulation in Acanthophrynus coronatus (Butler)(Amblypygi, Tarantulidae). Psyche 77:181–183CrossRefGoogle Scholar
  71. Starck VJ (1985) Stridulationsapparate einiger Spinnen–Morphologie und evolutionsbiologische Aspekte. J Zool Syst Evol Res 23:115–135CrossRefGoogle Scholar
  72. Stratton GE, Uetz GW (1983) Communication via substratum-coupled stridulation and reproductive isolation in wolf spiders (Araneae: Lycosidae). Anim Behav 31:164–172CrossRefGoogle Scholar
  73. Sueur J, Aubin T, Simonis C (2008) Seewave: a free modular tool for sound analysis and synthesis. Bioacoustics 18:213–226CrossRefGoogle Scholar
  74. Surlykke A, Kalko EK (2008) Echolocating bats cry out loud to detect their prey. PLoS One 3:e2036CrossRefPubMedPubMedCentralGoogle Scholar
  75. Suter RB, Keiley M (1984) Agonistic interactions between male Frontinella pyramitela (Araneae, Linyphiidae). Behav Ecol Sociobiol 15:1–7CrossRefGoogle Scholar
  76. Toft S, Wise DH (1999) Growth, development, and survival of a generalist predator fed single- and mixed species diets of different quality. Oecologia 119:191–197CrossRefPubMedGoogle Scholar
  77. Turnbull AL (1973) Ecology of the true spiders (Araneomorphae). Annu Rev Entomol 18:305–348CrossRefGoogle Scholar
  78. Uetz GW, Stratton GE (1982) Acoustic communication and reproductive isolation in spiders. In: Witt PN, Rovner JS (eds) Spider communication: mechanisms and ecological significance. Princeton University Press, New Jersey, pp 123–159Google Scholar
  79. Uhl G, Elias DO (2011) Communication. In: Herberstein ME (ed) Spider behavior: flexibility and versatility. Cambridge University Press, Cambridge, pp 127–190CrossRefGoogle Scholar
  80. Uhl G, Schmitt M (1996) Stridulation in Palpimanus gibbulus Dufour (Araneae: Palpimanidae). Rev Suisse Zool 2:649–660Google Scholar
  81. Wessel A (2006) Stridulation in the Coleoptera—an overview. In: Drosopoulos S, Claridge MF (eds) Insect Sounds and Communication. Physiology, Behaviour, Ecology and Evolution. CRC Press, Boca Raton, pp 397–403Google Scholar
  82. Wignall AE, Herberstein ME (2013) Male courtship vibrations delay predatory behaviour in female spiders. Sci Rep 3:3557CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wilder SM, Rypstra AL (2010) Males make poor meals: a comparison of nutrient extraction during sexual cannibalism and predation. Oecologia 162:617–625CrossRefPubMedGoogle Scholar
  84. Wise DH (2006) Cannibalism, food limitation, intraspecific competition, and the regulation of spider populations. Annu Rev Entomol 51:441–465CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  2. 2.Department of Zoology, Faculty of SciencesCharles UniversityPrahaCzech Republic

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