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Altruism during predation in an assassin bug

Naturwissenschaften volume 100, pages 913–922 (2013)Cite this article

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.

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References

  • Ables JR (1975) Notes on the biology of the predacious pentatomid Euthyrhynchus floridanus (L.). J Georgia Entomol Soc 10:353–356

    Google Scholar 

  • Bailey I, Myatt JP, Wilson AM (2013) Group hunting within the Carnivora: physiological, cognitive and environmental influences on strategy and cooperation. Behav Ecol Sociobiol 67:1–17

    Article  Google Scholar 

  • 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 320:1007–1012

    Article  Google Scholar 

  • Betz O, Kölsch G (2004) The role of adhesion in prey capture and predator defence in arthropods. Arthropod Struct Develop 33:3–30

    Article  Google Scholar 

  • Carter GG, Wilkinson GS (2013) Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment. Proc R Soc, Biol Sc 280:20122573

    Article  Google Scholar 

  • 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 39–78

    Google Scholar 

  • Cogni R, Freitas AVL, Amaral Filho BF (2002) Influence of prey size on predation success by Zelus longipes L. (Het., Reduviidae). J Appl Entomol 126:74–78

    Article  Google Scholar 

  • 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 499:256–261

    PubMed  Article  CAS  Google Scholar 

  • Coulson J, Coulson T (1995) Group hunting by Harris’ hawks in Texas. J Rapt Res 29:265–267

    Google Scholar 

  • de Waal FBM (2006) Fishy cooperation. PLoS Biol 4:e444

    PubMed  Article  Google Scholar 

  • Dejean A (2011) Prey capture behavior in an arboreal African ponerine ant. PLoS ONE 6:e19837

    PubMed  Article  CAS  Google Scholar 

  • 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 99:265–273

    PubMed  Article  CAS  Google Scholar 

  • 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:e59405

    PubMed  Article  CAS  Google Scholar 

  • Dejean A, Solano PJ, Ayroles J, Corbara B, Orivel J (2005) Arboreal ants build a trap to ambush and capture prey. Nature 434:973

    PubMed  Article  CAS  Google Scholar 

  • 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 41:21–24

    Google Scholar 

  • Forero D, Choe D-H, Weirauch C (2011) Resin gathering in neotropical resin bugs (Insecta: Hemiptera: Reduviidae): functional and comparative morphology. J Morphol 272:204–229

    PubMed  Article  Google Scholar 

  • Forthman M, Weirauch C (2012) Toxic associations: a review of the predatory behaviors of millipede assassin bugs (Hemiptera: Reduviidae: Ectrichodiinae). Eur J Entomol 109:147–153

    Google Scholar 

  • Grangier J, Dejean A, Malé P-J G, Orivel J (2008a) Indirect defense in a highly specific ant-plant mutualism. Naturwissenschaften 95:909–916

    PubMed  Article  CAS  Google Scholar 

  • Grangier J, Orivel J, Negrini M, Dejean A (2008b) Low intraspecific aggressiveness in two obligate plant-ant species. Insect Soc 55:238–240

    Article  Google Scholar 

  • Grégoire J-C (1988) Larval gregariousness in the Chrysomelidae. In: Jolivet P, Petitpierre E, Hsiao T (eds) The biology of Chrysomelidae. Junk, Dordrecht, pp 251–258

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behavior. I, II. J Theor Biol 7:1–52

    PubMed  Article  CAS  Google Scholar 

  • 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) 96:485–497

    Article  Google Scholar 

  • Haridass ET, Noble Morrison M, Balu A (1988) Predatory behavior of Rhynocoris marginatus Fabricius (Harpactorinae-Reduviidae-Heteroptera-Insecta). Proc Indian Acad Sc (Anim Sc) 97:41–48

    Article  Google Scholar 

  • Hwang WS, Weirauch C (2012) Evolutionary history of assassin bugs (Insecta: Hemiptera: Reduviidae): insights from divergence dating and ancestral state reconstruction. PLoS ONE 7:e45523

    PubMed  Article  CAS  Google Scholar 

  • Inoue H (1982) Studies on the mode of foraging of the gregarious assassin bug Agriosphodrus dohrni Signoret. Res Pop Ecol 24:211–223

    Article  Google Scholar 

  • Inoue H (1983) Nymphal cannibalism in relation to oviposition behavior of adults in the assassin bug, Agriosphodrus dohrni Signoret. Res Pop Ecol 25:189–197

    Article  Google Scholar 

  • Inoue H (1985) Group predatory behavior by the assassin bug Agriosphodrus dohrni Signoret (Hemiptera: Reduviidae). Res Pop Ecol 27:255–264

    Article  Google Scholar 

  • 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 10:82

  • Janz N (2002) Evolutionary ecology of oviposition strategies. In: Hilker M, Meiners T (eds) Chemoecology of insect eggs and egg deposition. Blackwell, Berlin, pp 349–376

    Google Scholar 

  • Jolivet P (2008) Cycloalexy. In: Capinera JL (ed) Encyclopedia of entomology. Springer, Berlin, pp 1139–1140

    Google Scholar 

  • 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:e56503

    PubMed  Article  Google Scholar 

  • 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 273:1523–1528

    Article  Google Scholar 

  • 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 103:771–774

    Article  Google Scholar 

  • 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 203–222

    Google Scholar 

  • 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 125–131

    Google Scholar 

  • 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 12:102

    Google Scholar 

  • Nomakuchi S, Yanagi T, Baba N, Takahira A, Hironaka M, Filippi L (2012) Provisioning call by mothers of a subsocial shield bug. J Zool 288:50–56

    Article  Google Scholar 

  • Pike N (2011) Using false discovery rates for multiple comparisons in ecology and evolution. Methods Ecol Evol 2:278–282

    Article  Google Scholar 

  • 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:e13110

    PubMed  Article  Google Scholar 

  • 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 17:486–490

    Article  CAS  Google Scholar 

  • Schaefer CW (2003) Prosorrhyncha (Heteroptera and Coleorrhyncha). In: Resh VH, Cardé RT (eds) Encyclopedia of insects. Academic, San Diego, pp 947–965

    Google Scholar 

  • 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 26:51–62

    PubMed  Article  CAS  Google Scholar 

  • 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 85:941–947

    Article  Google Scholar 

  • Stevens JR, Gilby IC (2004) A conceptual framework for nonkin food sharing: timing and currency of benefits. Anim Behav 67:603–614

    Article  Google Scholar 

  • Tan J, Hare B (2013) Bonobos share with strangers. PLoS ONE 8:e51922

    PubMed  Article  CAS  Google Scholar 

  • 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 19:1169–1180

    Google Scholar 

  • 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 95:641–649

    Article  Google Scholar 

  • 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 94:457–461

    Article  Google Scholar 

  • Wilson EO (1971) The insect societies. Belknap Press of Harvard University, Cambridge

    Google Scholar 

  • Yip EC, Rayor LS (2013) The influence of siblings on body condition in a social spider: is prey sharing cooperation or competition? Anim Behav 85:1161–1168

    Article  Google Scholar 

  • Zhang G, Weirauch C (2013) Sticky predators: a comparative study of sticky glands in harpactorine assassin bugs (Insecta: Hemiptera: Reduviidae). Acta Zool 94:1–10

    Article  CAS  Google Scholar 

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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 2007–2013 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.

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Authors and Affiliations

  1. Écologie des Forêts de Guyane, Campus agronomique, BP 316, 97379, Kourou cedex, France

    Alain Dejean

  2. Université de Toulouse; UPS, Ecolab, 118 route de Narbonne, 31062, Toulouse, France

    Alain Dejean

  3. National Research Council of Canada, 6100 Royalmount Avenue, Montreal, Quebec, H4P 2R2, Canada

    Messika Revel

  4. Centre INRS, Institut Armand-Frappier, Université du Québec, Laval, Quebec, H7V 1B7, Canada

    Messika Revel

  5. CNRS, Laboratoire Écologie Fonctionnelle et Environnement (UMR-CNRS 5245), 31062, Toulouse, France

    Frédéric Azémar

  6. Université de Toulouse; UPS, INP, Ecolab, 118 route de Narbonne, 31062, Toulouse, France

    Frédéric Azémar

  7. IRD; Maladies Infectieuses et Vecteurs, Ecologie, Génétique, Evolution et Contrôle (UMR-IRD 224), Équipe BEES, IRD 01, BP 171, Bobo-Dioulasso, Burkina Faso

    Olivier Roux

Authors
  1. Alain Dejean
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  2. Messika Revel
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  3. Frédéric Azémar
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  4. Olivier Roux
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Correspondence to Alain Dejean.

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Communicated by: Sven Thatje

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Dejean, A., Revel, M., Azémar, F. et al. Altruism during predation in an assassin bug. Naturwissenschaften 100, 913–922 (2013). https://doi.org/10.1007/s00114-013-1091-9

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  • DOI: https://doi.org/10.1007/s00114-013-1091-9

Keywords

  • Conspecific tolerance
  • Predation
  • Prey sharing
  • Reduviidae
  • Zelus annulosus