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Naturwissenschaften

, Volume 100, Issue 10, pp 913–922 | Cite as

Altruism during predation in an assassin bug

  • Alain Dejean
  • Messika Revel
  • Frédéric Azémar
  • Olivier Roux
Original Paper

Abstract

Zelus annulosus is an assassin bug species mostly noted on Hirtella physophora, a myrmecophyte specifically associated with the ant Allomerus decemarticulatus known to build traps on host tree twigs to ambush insect preys. The Z. annulosus females lay egg clutches protected by a sticky substance. To avoid being trapped, the first three instars of nymphs remain grouped in a clutch beneath the leaves on which they hatched, yet from time to time, they climb onto the upper side to group ambush preys. Long-distance prey detection permits these bugs to capture flying or jumping insects that alight on their leaves. Like some other Zelus species, the sticky substance of the sundew setae on their forelegs aids in prey capture. Group ambushing permits early instars to capture insects that they then share or not depending on prey size and the hunger of the successful nymphs. Fourth and fifth instars, with greater needs, rather ambush solitarily on different host tree leaves, but attract siblings to share large preys. Communal feeding permits faster prey consumption, enabling small nymphs to return sooner to the shelter of their leaves. By improving the regularity of feeding for each nymph, it likely regulates nymphal development, synchronizing molting and subsequently limiting cannibalism.

Keywords

Conspecific tolerance Predation Prey sharing Reduviidae Zelus annulosus 

Notes

Acknowledgments

We are grateful to Andrea Yockey-Dejean for proofreading the manuscript and the Laboratoire Environnement de Petit Saut for furnishing logistical help. Financial support for this study was partially provided by a fellowship from the French Investissement d’Avenir grant managed by the Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-0025), project Tri-Nutri, and by the Programme Convergence 20072013 Région Guyane (project Bi-APPLI) from the European Community.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The experiments comply with the current laws of the country in which they were conducted.

References

  1. Ables JR (1975) Notes on the biology of the predacious pentatomid Euthyrhynchus floridanus (L.). J Georgia Entomol Soc 10:353–356Google Scholar
  2. Bailey I, Myatt JP, Wilson AM (2013) Group hunting within the Carnivora: physiological, cognitive and environmental influences on strategy and cooperation. Behav Ecol Sociobiol 67:1–17CrossRefGoogle Scholar
  3. Bérenger J-M, Plutot-Sigwalt D (1997) Relations privilégiées de certains Heteroptera Reduviidae prédateur avec les végétaux. Premier cas connu d’un Harpactorinae phytophage. C R Acad Sci 320:1007–1012CrossRefGoogle Scholar
  4. Betz O, Kölsch G (2004) The role of adhesion in prey capture and predator defence in arthropods. Arthropod Struct Develop 33:3–30CrossRefGoogle Scholar
  5. Carter GG, Wilkinson GS (2013) Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proc R Soc, Biol Sc 280:20122573CrossRefGoogle Scholar
  6. Cerda X, Dejean A (2011) Predation by ants on arthropods and other animals. In: Polidori C (ed) Predation in the Hymenoptera: an evolutionary perspective. Transworld Research Network, Trivandrum, pp 39–78Google Scholar
  7. Cogni R, Freitas AVL, Amaral Filho BF (2002) Influence of prey size on predation success by Zelus longipes L. (Het., Reduviidae). J Appl Entomol 126:74–78CrossRefGoogle Scholar
  8. Corzo G, Adachi-Akahane S, Nagao T, Kusui Y, Nakajima T (2001) Novel peptides from assassin bugs (Hemiptera: Reduviidae): isolation, chemical and biological characterization. FEBS Lett 499:256–261PubMedCrossRefGoogle Scholar
  9. Coulson J, Coulson T (1995) Group hunting by Harris’ hawks in Texas. J Rapt Res 29:265–267Google Scholar
  10. de Waal FBM (2006) Fishy cooperation. PLoS Biol 4:e444PubMedCrossRefGoogle Scholar
  11. Dejean A (2011) Prey capture behavior in an arboreal African ponerine ant. PLoS ONE 6:e19837PubMedCrossRefGoogle Scholar
  12. Dejean A, Carpenter JM, Corbara B, Wright P, Roux O, LaPierre LM (2012) The hunter becomes the hunted: when cleptobiotic insects are captured by their target ants. Naturwissenschaften 99:265–273PubMedCrossRefGoogle Scholar
  13. Dejean A, Orivel J, Rossi V, Roux O, Lauth J, Malé P-J G, Céréghino R, Leroy C (2013) Predation success by a plant-ant indirectly favours the growth and fitness of its host myrmecophyte. PLoS ONE 8:e59405PubMedCrossRefGoogle Scholar
  14. Dejean A, Solano PJ, Ayroles J, Corbara B, Orivel J (2005) Arboreal ants build a trap to ambush and capture prey. Nature 434:973PubMedCrossRefGoogle Scholar
  15. Edwards JS (1966) Observations on the life history and predatory behaviour of Zelus exsanguis (Stål) (Heteroptera: Reduviidae). Proc R Entomol Soc London, Series A, Gen Entomol 41:21–24Google Scholar
  16. Forero D, Choe D-H, Weirauch C (2011) Resin gathering in neotropical resin bugs (Insecta: Hemiptera: Reduviidae): functional and comparative morphology. J Morphol 272:204–229PubMedCrossRefGoogle Scholar
  17. Forthman M, Weirauch C (2012) Toxic associations: a review of the predatory behaviors of millipede assassin bugs (Hemiptera: Reduviidae: Ectrichodiinae). Eur J Entomol 109:147–153Google Scholar
  18. Grangier J, Dejean A, Malé P-J G, Orivel J (2008a) Indirect defense in a highly specific ant-plant mutualism. Naturwissenschaften 95:909–916PubMedCrossRefGoogle Scholar
  19. Grangier J, Orivel J, Negrini M, Dejean A (2008b) Low intraspecific aggressiveness in two obligate plant-ant species. Insect Soc 55:238–240CrossRefGoogle Scholar
  20. Grégoire J-C (1988) Larval gregariousness in the Chrysomelidae. In: Jolivet P, Petitpierre E, Hsiao T (eds) The biology of Chrysomelidae. Junk, Dordrecht, pp 251–258Google Scholar
  21. Hamilton WD (1964) The genetical evolution of social behavior. I, II. J Theor Biol 7:1–52PubMedCrossRefGoogle Scholar
  22. Haridass ET, Balu A, Noble Morrison M (1987) Feeding and behavioural parameters and egg ultrastructure in the biosystematic of Reduviidae. Proc Indian Acad Sc (Anim Sc) 96:485–497CrossRefGoogle Scholar
  23. Haridass ET, Noble Morrison M, Balu A (1988) Predatory behavior of Rhynocoris marginatus Fabricius (Harpactorinae-Reduviidae-Heteroptera-Insecta). Proc Indian Acad Sc (Anim Sc) 97:41–48CrossRefGoogle Scholar
  24. Hwang WS, Weirauch C (2012) Evolutionary history of assassin bugs (Insecta: Hemiptera: Reduviidae): insights from divergence dating and ancestral state reconstruction. PLoS ONE 7:e45523PubMedCrossRefGoogle Scholar
  25. Inoue H (1982) Studies on the mode of foraging of the gregarious assassin bug Agriosphodrus dohrni Signoret. Res Pop Ecol 24:211–223CrossRefGoogle Scholar
  26. Inoue H (1983) Nymphal cannibalism in relation to oviposition behavior of adults in the assassin bug, Agriosphodrus dohrni Signoret. Res Pop Ecol 25:189–197CrossRefGoogle Scholar
  27. Inoue H (1985) Group predatory behavior by the assassin bug Agriosphodrus dohrni Signoret (Hemiptera: Reduviidae). Res Pop Ecol 27:255–264CrossRefGoogle Scholar
  28. Jackson RR, Salm K, Nelson XJ (2010) Specialized prey selection behavior of two East African assassin bugs, Scipinnia repax and Nagusta sp. that prey on social jumping spiders. J Insect Sc 10:82Google Scholar
  29. Janz N (2002) Evolutionary ecology of oviposition strategies. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, pp 349–376Google Scholar
  30. Jolivet P (2008) Cycloalexy. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Berlin, pp 1139–1140Google Scholar
  31. Kavčič A, Čokl A, Laumann RA, Blassioli-Moraes MC, Borges M (2013) Tremulatory and abdomen vibration signals enable communication through air in the stink bug Euschistus heros. PLoS ONE 8:e56503PubMedCrossRefGoogle Scholar
  32. Kölliker M, Chuckalovcak JP, Haynes KF, Brodie ED (2006) Maternal food provisioning in relation to condition-dependent offspring odours in burrower bugs (Sehirus cinctus). Proc R Soc, Biol Sc 273:1523–1528CrossRefGoogle Scholar
  33. Law YH, Sediqi A (2010) Sticky substance on eggs improves predation success and substrate adhesion in newly hatched Zelus renardii (Hemiptera: Reduviidae) instars. Ann Entomol Soc Amer 103:771–774CrossRefGoogle Scholar
  34. Leimar O, Connor RC (2003) By-product benefits, reciprocity, and pseudoreciprocity in mutualism. In: Hammerstein P (ed) Genetic and cultural evolution of cooperation. MIT, Cambridge, pp 203–222Google Scholar
  35. Maran SPM, Ambrose DP (2000) Paralytic potential of Catamiarus brevipennis (Serville), a potential biological control agent (Insecta: Heteroptera: Reduviidae). In: Ignacimuth A, Sen A, Janarthanan S (eds) Biotechnological applications for integrated pest management. Oxford, New Delhi, pp 125–131Google Scholar
  36. Moore MP, Burt CR, Whitney TD, Hastings SA, Chang GC (2012) Does social feeding improve larval survival of the two-spotted lady beetle, Adalia bipunctata? J Ins Sc 12:102Google Scholar
  37. Nomakuchi S, Yanagi T, Baba N, Takahira A, Hironaka M, Filippi L (2012) Provisioning call by mothers of a subsocial shield bug. J Zool 288:50–56CrossRefGoogle Scholar
  38. Pike N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2:278–282CrossRefGoogle Scholar
  39. Revel M, Dejean A, Céréghino R, Roux O (2010) An assassin among predators: the relationship between plant-ants, their host myrmecophytes and the Reduviidae Zelus annulosus. PloS ONE 5:e13110PubMedCrossRefGoogle Scholar
  40. Sahayaraj K, Vinothkanna (2011) Insecticidal activity of venomous saliva from Rhynocoris fuscipes (Reduviidae) against Spodoptera litura and Helicoverpa armigera by microinjection and oral administration. J Venom Anim Toxins incl Trop Dis 17:486–490CrossRefGoogle Scholar
  41. Schaefer CW (2003) Prosorrhyncha (Heteroptera and Coleorrhyncha). In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Academic, San Diego, pp 947–965Google Scholar
  42. Settepani V, Grinsted L, Granfeldt J, Jensen JL, Bilde T (2013) Task specialization in two social spiders, Stegodyphus sarasinorum (Eresidae) and Anelosimus eximius (Theridiidae). J Evol Biol 26:51–62PubMedCrossRefGoogle Scholar
  43. Silk JB, Brosnan SF, Henrich J, Lambeth SP, Shapiro S (2013) Chimpanzees share food for many reasons: the role of kinship, reciprocity, social bonds and harassment on food transfers. Anim Behav 85:941–947CrossRefGoogle Scholar
  44. Stevens JR, Gilby IC (2004) A conceptual framework for nonkin food sharing: timing and currency of benefits. Anim Behav 67:603–614CrossRefGoogle Scholar
  45. Tan J, Hare B (2013) Bonobos share with strangers. PLoS ONE 8:e51922PubMedCrossRefGoogle Scholar
  46. Weirauch C (2006) Observations on the sticky trap predator Zelus luridus Stål (Heteroptera, Reduviidae, Harpactorinae), with the description of a novel gland associated with the female genitalia. Denisia 19:1169–1180Google Scholar
  47. Weirauch C, Alvarez C, Zhang G (2012) Zelus renardii and Z. tetracanthus (Hemiptera: Reduviidae): biological attributes and the potential for dispersal in two assassin bug species. Fl Entomol 95:641–649CrossRefGoogle Scholar
  48. Werner W, Reid W (2001) Surface morphology of legs in the assassin bug Zelus longipes (Hemiptera: Reduviidae): a scanning electron microscopy study with an emphasis on hairs and pores. Ann Entomol Soc Amer 94:457–461CrossRefGoogle Scholar
  49. Wilson EO (1971) The insect societies. Belknap Press of Harvard University, CambridgeGoogle Scholar
  50. Yip EC, Rayor LS (2013) The influence of siblings on body condition in a social spider: is prey sharing cooperation or competition? Anim Behav 85:1161–1168CrossRefGoogle Scholar
  51. Zhang G, Weirauch C (2013) Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae). Acta Zool 94:1–10CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Alain Dejean
    • 1
    • 2
  • Messika Revel
    • 3
    • 4
  • Frédéric Azémar
    • 5
    • 6
  • Olivier Roux
    • 7
  1. 1.Écologie des Forêts de GuyaneKourou cedexFrance
  2. 2.Université de Toulouse; UPS, EcolabToulouseFrance
  3. 3.National Research Council of CanadaMontrealCanada
  4. 4.Centre INRS, Institut Armand-FrappierUniversité du QuébecLavalCanada
  5. 5.CNRSLaboratoire Écologie Fonctionnelle et Environnement (UMR-CNRS 5245)ToulouseFrance
  6. 6.Université de Toulouse; UPS, INP, EcolabToulouseFrance
  7. 7.IRD; Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle (UMR-IRD 224)Bobo-DioulassoBurkina Faso

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