1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Entomology
  4. Volume 68, 2023
  5. Article

Annual Review of Entomology

Volume 68, 2023

The Biology and Ecology of Parasitoid Wasps of Predatory Arthropods

Abstract

Parasitoid wasps are important components of insect food chains and have played a central role in biological control programs for over a century. Although the vast majority of parasitoids exploit insect herbivores as hosts, others parasitize predatory insects and arthropods, such as ladybird beetles, hoverflies, lacewings, ground beetles, and spiders, or are hyperparasitoids. Much of the research on the biology and ecology of parasitoids of predators has focused on ladybird beetles, whose parasitoids may interfere with the control of insect pests like aphids by reducing ladybird abundance. Alternatively, parasitoids of the invasive ladybird may reduce its harmful impact on native ladybird populations. Different life stages of predatory insects and spiders are susceptible to parasitism to different degrees. Many parasitoids of predators exhibit intricate physiological interrelationships with their hosts, adaptively manipulating host behavior, biology, and ecology in ways that increase parasitoid survival and fitness.

Keyword(s): biological control, ladybird, natural enemy, spiders, trophic cascade
Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-120120-111607
2023-01-23
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/ento/68/1/annurev-ento-120120-111607.html?itemId=/content/journals/10.1146/annurev-ento-120120-111607&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adamo SA. 2019. Turning your victim into a collaborator: exploitation of insect behavioral control systems by parasitic manipulators. Curr. Opin. Insect Sci. 33:25–29
     [Google Scholar]
  2. 2.
    Al Abassi S, Birkett MA, Pettersson J, Pickett JA, Wadhams LJ, Woodcock CM 2001. Response of the ladybird parasitoid Dinocampus coccinellae to toxic alkaloids from the seven-spot ladybird, Coccinella septempunctata. J. Chem. Ecol. 27:33–43
     [Google Scholar]
  3. 3.
    Al Rouechdi K, Panis A 1981. Les parasites de Chrysoperla carnea Steph. (Neuroptera, Chrysopidae) sur Olivier en Provence. Agronomie 1:139–41
     [Google Scholar]
  4. 4.
    Andersen J, Skorping A. 1991. Parasites of carabid beetles: prevalence depends on habitat selection of the host. Can. J. Zool. 69:1216–20
     [Google Scholar]
  5. 5.
    Austin A. 1984. The fecundity, development and host relationships of Ceratobaeus spp. (Hymenoptera: Scelionidae), parasites of spider eggs. Ecol. Entomol. 9:125–38
     [Google Scholar]
  6. 6.
    Austin AD. 1985. The function of spider egg sacs in relation to parasitoids and predators, with special reference to the Australian fauna. J. Nat. Hist. 19:359–76
     [Google Scholar]
  7. 7.
    Ayre GL. 1962. Pseudometagea schwarzii (Ashm.) (Eucharitidae: Hymenoptera), a parasite of Lasius neoniger Emery (Formicidae: Hymenoptera). Can. J. Zool. 40:157–64
     [Google Scholar]
  8. 8.
    Barron JR. 1987. Adults and larvae of two new species of Gelis (Hymenoptera: Ichneumonidae) parasitizing eggs of spiders Agelenopsis potteri (Araneae: Agelenidae) and Lycosa rabida (Araneae: Lycosidae). Ann. Entomol. Soc. Am. 80:21–28
     [Google Scholar]
  9. 9.
    Beckage NE, Gelman DB. 2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49:299–330
     [Google Scholar]
  10. 10.
    Benamú MA, Lacava M, García LF, Santana M, Viera C 2017. Spiders associated with agroecosystems: roles and perspectives. Behaviour and Ecology of Spiders C Viera, MO Gonzaga 275–302 Berlin: Springer
     [Google Scholar]
  11. 11.
    Berkvens N, Moens J, Berkvens D, Samih MA, Tirry L, De Clercq P. 2010. Dinocampus coccinellae as a parasitoid of the invasive ladybird Harmonia axyridis in Europe. Biol. Control 53:92–99
     [Google Scholar]
  12. 12.
    Bjørnson S. 2008. Natural enemies of the convergent lady beetle, Hippodamia convergens Guérin-Méneville: their inadvertent importation and potential significance for augmentative biological control. Biol. Control 44:305–11
     [Google Scholar]
  13. 13.
    Bowden J, Buddle C. 2012. Egg sac parasitism of Arctic wolf spiders (Araneae: Lycosidae) from northwestern North America. J. Arachnol. 40:348–50
     [Google Scholar]
  14. 14.
    Brown PM, Thomas CE, Lombaert E, Jeffries DL, Estoup A, Handley L-JL. 2011. The global spread of Harmonia axyridis (Coleoptera: Coccinellidae): distribution, dispersal and routes of invasion. BioControl 56:623–41
     [Google Scholar]
  15. 15.
    Cartwright B, Eikenbary RD, Angalet GW. 1982. Parasitism by Perilitus coccinellae [Hym.: Braconidae] of indigenous coccinellid hosts and the introduced Coccinella septempunctata [Col.: Coccinellidae], with notes on winter mortality. Entomophaga 27:237–43
     [Google Scholar]
  16. 16.
    Ceryngier P. 2000. Overwintering of Coccinella septempunctata (Coleoptera: Coccinellidae) at different altitudes in the Karkonosze Mts, SW Poland. Eur. J. Entomol. 97:323–28
     [Google Scholar]
  17. 17.
    Ceryngier P, Hodek I 1996. Enemies of Coccinellidae. Ecology of Coccinellidae I Hodek, A Honěk 319–50 Berlin: Springer
     [Google Scholar]
  18. 18.
    Ceryngier P, Nedvěd O, Grez AA, Riddick EW, Roy HE et al. 2018. Predators and parasitoids of the harlequin ladybird, Harmonia axyridis, in its native range and invaded areas. Biol. Invasions 20:1009–31
     [Google Scholar]
  19. 19.
    Ceryngier P, Roy HE, Poland RL 2012. Natural enemies of ladybird beetles. Ecology and Behaviour of the Ladybird Beetles (Coccinellidae) I Hodek, HF van Emden, A Honěk 375–443 Oxford, UK: Blackwell
     [Google Scholar]
  20. 20.
    Clausen CP. 1940. The oviposition habits of the Eucharidae (Hymenoptera). J. Wash. Acad. Sci. 30:504–16
     [Google Scholar]
  21. 21.
    Cobb LM, Cobb VA. 2004. Occurrence of parasitoid wasps, Baeus sp. and Gelis sp., in the egg sacs of the wolf spiders Pardosa moesta and Pardosa sternalis (Araneae, Lycosidae) in southeastern Idaho. Can. Field-Nat. 118:122–23
     [Google Scholar]
  22. 22.
    Comont RF, Purse BV, Phillips W, Kunin WE, Hanson M et al. 2014. Escape from parasitism by the invasive alien ladybird, Harmonia axyridis. Insect Conserv. Divers. 7:334–42
     [Google Scholar]
  23. 23.
    Critchley B. 1973. Parasitism of the larvae of some Carabidae (Coleoptera). J. Entomol. 48:37–42
     [Google Scholar]
  24. 24.
    Daloze D, Braekman J-C, Pasteels JM. 1994. Ladybird defence alkaloids: structural, chemotaxonomic and biosynthetic aspects (Col.: Coccinellidae). . Chemoecology 5173–83
  25. 25.
    Davis DS, Stewart SL, Manica A, Majerus ME. 2006. Adaptive preferential selection of female coccinellid hosts by the parasitoid wasp Dinocampus coccinellae (Hymenoptera: Braconidae). Eur. J. Entomol. 103:41–45
     [Google Scholar]
  26. 26.
    de Castro-Guedes C, de Almeida L. 2016. Laboratory investigations reveal that Harmonia axyridis (Coleoptera: Coccinellidae) is a poor host for Dinocampus coccinellae (Hymenoptera: Braconidae) in Brazil. J. Insect Sci. 16:e55
     [Google Scholar]
  27. 27.
    De La Filia AG, Bain SA, Ross L 2015. Haplodiploidy and the reproductive ecology of Arthropods. Curr. Opin. Insect Sci. 9:36–43
     [Google Scholar]
  28. 28.
    Devetak D, Klokocovnik V. 2016. The feeding biology of adult lacewings (Neuroptera): a review. Trends Entomol. 12:29–42
     [Google Scholar]
  29. 29.
    Dheilly NM, Maure F, Ravallec M, Galinier R, Doyon J et al. 2015. Who is the puppet master? Replication of a parasitic wasp-associated virus correlates with host behaviour manipulation. Proc. R. Soc. Biol. Sci. B 282:e20142773
     [Google Scholar]
  30. 30.
    Dimitrov D, Hormiga G. 2021. Spider diversification through space and time. Annu. Rev. Entomol. 66:225–41
     [Google Scholar]
  31. 31.
    Dindo ML, Francati S, Lanzoni A, Di Vitantonio C, Marchetti E et al. 2016. Interactions between the multicolored Asian lady beetle Harmonia axyridis and the parasitoid Dinocampus coccinellae. Insects 7:e67
     [Google Scholar]
  32. 32.
    Dixon AFG, Hemptinne JL, Kindlmann P. 1997. Effectiveness of ladybirds as biological control agents: patterns and processes. Entomophaga 42:71–83
     [Google Scholar]
  33. 33.
    Drummond F, Choate B. 2011. Ants as biological control agents in agricultural cropping systems. Terr. Arthropod Rev. 4:157–80
     [Google Scholar]
  34. 34.
    Dunn L, Lequerica M, Reid CR, Latty T. 2020. Dual ecosystem services of syrphid flies (Diptera: Syrphidae): pollinators and biological control agents. Pest Manag. Sci. 76:1973–79
     [Google Scholar]
  35. 35.
    Eason RR, Peck WB, Whitcomb W. 1967. Notes on spider parasites, including a reference list. J. Kans. Entomol. Soc. 40:422–34
     [Google Scholar]
  36. 36.
    Eberhard WG. 2000. Spider manipulation by a wasp larva. Nature 406:255–56
     [Google Scholar]
  37. 37.
    Edgar WD. 1971. Aspects of the ecology and energetics of the egg sac parasites of the wolf spider Pardosa lugubris (Walckenaer). Oecologia 7:155–63
     [Google Scholar]
  38. 38.
    Feener DH. 2000. Is the assembly of ant communities mediated by parasitoids?. Oikos 90:79–88
     [Google Scholar]
  39. 39.
    Fei M, Hu H, Gols R, Liu S, Wan X et al. 2021. Development and oviposition strategies in two congeneric gregarious larval-pupal endoparasitoids of the seven-spot ladybird, Coccinella septempunctata. Biol. Control 163:104756
     [Google Scholar]
  40. 40.
    Fernandez-Fournier P, Straus S, Sharpe R, Avilés L. 2019. Behavioural modification of a social spider by a parasitoid wasp. Ecol. Entomol. 44:157–62
     [Google Scholar]
  41. 41.
    Fink LS. 1987. Green lynx spider egg sacs: sources of mortality and the function of female guarding (Araneae, Oxyopidae). J. Arachnol. 15:231–39
     [Google Scholar]
  42. 42.
    Firlej A, Lucas E, Coderre D, Boivin G. 2007. Teratocytes growth pattern reflects host suitability in a host-parasitoid assemblage. Physiol. Entomol. 32:181–87
     [Google Scholar]
  43. 43.
    Firlej A, Lucas E, Coderre D, Boivin G. 2010. Impact of host behavioral defenses on parasitization efficacy of a larval and adult parasitoid. BioControl 55:339–48
     [Google Scholar]
  44. 44.
    Fitton M, Rotheray G. 1982. A key to the European genera of diplazontine ichneumon-flies, with notes on the British fauna. Syst. Entomol. 7:311–20
     [Google Scholar]
  45. 45.
    Fitton M, Shaw MR, Austin A 1987. The Hymenoptera associated with spiders in Europe. Zool. J. Linn. Soc. 90:65–93
     [Google Scholar]
  46. 46.
    Gauld ID, Dubois J. 2006. Phylogeny of the Polysphincta group of genera (Hymenoptera: Ichneumonidae; Pimplinae): a taxonomic revision of spider ectoparasitoids. Syst. Entomol. 31:529–64
     [Google Scholar]
  47. 47.
    Geoghegan IE, Majerus T, Majerus ME. 1998. Differential parasitisation of adult and pre-imaginal Coccinella septempunctata (Coleoptera: Coccinellidae) by Dinocampus coccinellae (Hymenoptera: Braconidae). Eur. J. Entomol. 95:571–79
     [Google Scholar]
  48. 48.
    Gerling D, Bar D. 1985. Parasitization of Chysoperla carnea [Neuroptera, Chrysopidae] in cotton fields of Israel. Entomophaga 30:409–14
     [Google Scholar]
  49. 49.
    Gibson GAP. 2001. The Australian species of Pachyneuron Walker (Hymenoptera: Chalcidoidea: Pteromalidae). J. Hymenoptera Res. 10:29–54
     [Google Scholar]
  50. 50.
    Gilbert F. 2005. Syrphid aphidophagous predators in a food-web context. Eur. J. Entomol. 102:325–33
     [Google Scholar]
  51. 51.
    Giorgi JA, Vandenberg NJ, McHugh JV, Forrester JA, Ślipiński SA et al. 2009. The evolution of food preferences in Coccinellidae. Biol. Control 51:215–31
     [Google Scholar]
  52. 52.
    Godfray HCJ 1994. Parasitoids: Behavioral and Evolutionary Ecology Princeton, NJ: Princeton Univ. Press
  53. 53.
    Godfray HCJ, Shimada M. 1999. Parasitoids as model organisms for ecologists. Popul. Ecol. 41:3–10
     [Google Scholar]
  54. 54.
    Gonzaga MO, Sobczak JF. 2007. Parasitoid-induced mortality of Araneus omnicolor (Araneae, Araneidae) by Hymenoepimecis sp. (Hymenoptera, Ichneumonidae) in southeastern Brazil. Naturwissenschaften 94:223–27
     [Google Scholar]
  55. 55.
    Greco C. 1997. Specificity and instar preference of Diplazon laetatorius (Hym.: Ichneumonidae) parasitizing aphidophagous syrphids (Dipt.: Syrphidae). Entomophaga 42:315–18
     [Google Scholar]
  56. 56.
    Grosman AH, Janssen A, de Brito EF, Cordeiro EG, Colares F et al. 2008. Parasitoid increases survival of its pupae by inducing hosts to fight predators. PLOS ONE 3:e2276
     [Google Scholar]
  57. 57.
    Guo Q, Meng L, Fei M, Li B. 2021. Oviposition and development of the gregarious parasitoid Homalotylus eytelweinii (Hymenoptera: Encyrtidae) in relation to host stage of predaceous ladybirds. Biocontrol Sci. Technol. 32::455–66
     [Google Scholar]
  58. 58.
    Guzman LM, Germain RM, Forbes C, Straus S, O'Connor MI et al. 2019. Towards a multi-trophic extension of metacommunity ecology. Ecol. Lett. 22:19–33
     [Google Scholar]
  59. 59.
    Harvey JA. 2005. Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomol. Exp. Appl. 117:1–13
     [Google Scholar]
  60. 60.
    Harvey JA, Gols R, Tanaka T. 2011. Differing success of defense strategies in two parasitoid wasps in protecting their pupae against a secondary hyperparasitoid. Ann. Entomol. Soc. Am. 104:1005–11
     [Google Scholar]
  61. 61.
    Harvey JA, Tanaka T, Kruidhof M, Vet LEM, Gols R. 2011. The “usurpation hypothesis” revisited: Dying caterpillar repels attack from a hyperparasitoid wasp. Anim. Behav. 81:1281–87
     [Google Scholar]
  62. 62.
    Harvey JA, Visser B, Lammers M, Marien J, Gershenzon J et al. 2018. Ant-like traits in wingless parasitoids repel attack from wolf spiders. J. Chem. Ecol. 44:894–904
     [Google Scholar]
  63. 63.
    Harvey JA, Wagenaar R, Bezemer TM. 2009. Interactions to the fifth trophic level: Secondary and tertiary parasitoid wasps show extraordinary efficiency in utilizing host resources. J. Anim. Ecol. 78:686–92
     [Google Scholar]
  64. 64.
    Hayashi M, Nomura M. 2011. Larvae of the green lacewing Mallada desjardinsi (Neuroptera: Chrysopidae) protect themselves against aphid-tending ants by carrying dead aphids on their backs. App. Entomol. Zool. 46:407–13
     [Google Scholar]
  65. 65.
    Heimpel GE, Mills NJ. 2017. Biological Control: Ecology and Applications Cambridge, UK: Cambridge Univ. Press
  66. 66.
    Holland JM 2002. Carabid beetles: their ecology, survival and use in agroecosystems. The Agroecology of Carabid Beetles JM Holland 1–40 Andover, UK: Intercept Ltd.
     [Google Scholar]
  67. 67.
    Hoogendoorn M, Heimpel GE. 2002. Indirect interactions between an introduced and a native ladybird beetle species mediated by a shared parasitoid. Biol. Control 25:224–30
     [Google Scholar]
  68. 68.
    Huber JT 2017. Biodiversity of Hymenoptera. Insect Biodiversity: Science and Society R Foottit, PH Adler 419–61 Hoboken, NJ: Wiley
     [Google Scholar]
  69. 69.
    Jacometti M, Jørgensen N, Wratten S. 2010. Enhancing biological control by an omnivorous lacewing: Floral resources reduce aphid numbers at low aphid densities. Biol. Control 55:159–65
     [Google Scholar]
  70. 70.
    Jankowska B. 2004. Parasitoids of aphidophagous Syrphidae occurring in cabbage aphid (Brevicoryne brassicae L.) colonies on cabbage vegetables. J. Plant Prot. Res. 44:299–305
     [Google Scholar]
  71. 71.
    Jervis MA, Ellers J, Harvey JA. 2008. Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. Annu. Rev. Entomol. 53:361–85
     [Google Scholar]
  72. 72.
    Jervis MA, Kidd NAC. 1986. Host-feeding strategies in hymenopteran parasitoids. Biol. Rev. 61:395–434
     [Google Scholar]
  73. 73.
    Kadono-Okuda K, Sakurai H, Takeda S, Okuda T. 1995. Synchronous growth of a parasitoid, Perilitus coccinellae, and teratocytes with the development of the host, Coccinella septempunctata. Entomol. Exp. Appl. 75:145–49
     [Google Scholar]
  74. 74.
    Kamal M. 1926. A study of some hymenopterous parasites of aphidophagous Syrphidae. J. Econ. Entomol. 19:721–30
     [Google Scholar]
  75. 75.
    Kareem AA, Abbas MA, Aljaafari RK, Al-Zurfi SM, Mouhsan ZM. 2019. New report of hoverfly parasite Diplazon laetatorius (Fabricius, 1781) (Ichneumonidae-Hymenoptera) from Iraq. IOP Conference Series: Earth and Environmental Science, Vol. 388 The 4th International Conference on Agricultural Sciences (4thICAS), 17–18 November 2019, Agriculture College/University of Kerbala, Kerbala City, Iraq art. 388 Bristol, UK: IOP Publ.
     [Google Scholar]
  76. 76.
    Karut K, Kazak C, Arslan A, Şekeroğlu E. 2003. Natural parasitism of Chrysoperla carnea by hymenopterous parasitoids in cotton-growing areas of Çukurova, Turkey. Phytoparasitica 31:90–93
     [Google Scholar]
  77. 77.
    Kawatsu K, Ushio M, van Veen FF, Kondoh M. 2021. Are networks of trophic interactions sufficient for understanding the dynamics of multi-trophic communities? Analysis of a tri-trophic insect food-web time-series. Ecol. Lett. 24:543–52
     [Google Scholar]
  78. 78.
    Kessler A, Fokkinga A. 1973. Hymenopterous parasites in egg sacs of spiders of the genus Pardosa (Araneida, Lycosidae). Tijdschr. Entomol. 116:43–61
     [Google Scholar]
  79. 79.
    King J. 1919. Notes on the biology of the carabid genera Brachynus, Galerita and Chlaenius. Ann. Entomol. Soc. Am. 12:382–88
     [Google Scholar]
  80. 80.
    Klausnitzer B. 1969. Zur Kenntnis der Entomoparasiten mitteleuropaischer Coccinellidae. Abh. Ber. Naturkundemus. Görlitz 44:1–15
     [Google Scholar]
  81. 81.
    Klopfstein S. 2014. Revision of the Western Palaearctic Diplazontinae (Hymenoptera, Ichneumonidae). Zootaxa 3801:1–143
     [Google Scholar]
  82. 82.
    Kloss TG, Gonzaga MO, Roxinol JAM, Sperber CF. 2016. Host behavioural manipulation of two orb-weaver spiders by parasitoid wasps. Anim. Behav. 111:289–96
     [Google Scholar]
  83. 83.
    Knapp M, Řeřicha M, Maršíková S, Harabiš F, Kadlec T et al. 2019. Invasive host caught up with a native parasitoid: field data reveal high parasitism of Harmonia axyridis by Dinocampus coccinellae in Central Europe. Biol. Invasions 21:2795–802
     [Google Scholar]
  84. 84.
    Korenko S. 2017. First record from Italy of Zatypota anomala (Ichneumonidae, Ephialtini), a parasitoid of the cribellate spider Dictyna pusilla (Araneae, Dictynidae). Arachnol. Lett. 54:1–4
     [Google Scholar]
  85. 85.
    Korenko S, Korenková B, Satrapová J, Hamouzová K, Belgers D. 2015. Modification of Tetragnatha montana (Araneae, Tetragnathidae) web architecture induced by larva of the parasitoid Acrodactyla quadrisculpta (Hymenoptera, Ichneumonidae, Polysphincta genus-group). Zool. Stud. 54:e40
     [Google Scholar]
  86. 86.
    Korenko S, Pekár S. 2011. A parasitoid wasp induces overwintering behaviour in its spider host. PLOS ONE 6:e24628
     [Google Scholar]
  87. 87.
    Korenko S, Schmidt S, Schwarz M, Gibson GA, Pekar S. 2013. Hymenopteran parasitoids of the ant-eating spider Zodarion styliferum (Simon) (Araneae, Zodariidae). ZooKeys 262:e3857
     [Google Scholar]
  88. 88.
    Korenko S, Spasojevic T, Pekár S, Walter GH, Korenková V et al. 2018. One generalist or several specialist species? Wide host range and diverse manipulations of the hosts’ web-building behaviour in the true spider parasitoid Zatypota kauros (Hymenoptera: Ichneumonidae). Insect Conserv. Divers. 11:587–99
     [Google Scholar]
  89. 89.
    Kostro-Ambroziak A, Kupryjanowicz J, Schwarz M. 2020. Who wins? Ray spiders (Theridiosoma gemmosum) (Araneae: Theridiosomatidae) versus egg sac parasitoids. J. Arachnol. 48:90–93
     [Google Scholar]
  90. 90.
    Koyama S, Thomas CE, Takata M. 2013. Relationship between the size of the parasitoid wasp Dinocampus coccinellae (Hymenoptera: Braconidae) and host ladybird species (Coleoptera: Coccinellidae). Trends Entomol 9:39–43
     [Google Scholar]
  91. 91.
    Lachaud J-P, Pérez-Lachaud G. 2012. Diversity of species and behavior of Hymenopteran parasitoids of ants: a review. Psyche J. Entomol. 2012:e134746
     [Google Scholar]
  92. 92.
    Le Ralec A 1995. Egg contents in relation to host-feeding in some parasitic Hymenoptera. Entomophaga 40:87–93
     [Google Scholar]
  93. 93.
    Liere H, Perfecto I. 2014. Cheating on a mutualism: indirect benefits of ant attendance to a coccidophagous coccinellid. Environ. Entomol. 37:143–49
     [Google Scholar]
  94. 94.
    Lövei GL, Sunderland KD. 1996. Ecology and behavior of ground beetles (Coleoptera: Carabidae). Annu. Rev. Entomol. 41:231–56
     [Google Scholar]
  95. 95.
    Luff M. 1987. Biology of polyphagous ground beetles in agriculture. Agric. Zool. Rev. 2:237–78
     [Google Scholar]
  96. 96.
    Majerus MEN, Geoghegan IE, Majerus TMO. 2000. Adaptive preferential selection of young coccinellid hosts by the parasitoid wasp Dinocampus coccinellae (Hymenoptera: Braconidae). Eur. J. Entomol. 97:161–64
     [Google Scholar]
  97. 97.
    Majerus MEN, Sloggett JJ, Godeau J-F, Hemptinne J-L. 2007. Interactions between ants and aphidophagous and coccidophagous ladybirds. Popul. Ecol. 49:15–27
     [Google Scholar]
  98. 98.
    Marie J, Vetter RS 2015. Establishment of the brown widow spider (Araneae: Theridiidae) and infestation of its egg sacs by a parasitoid, Philolema latrodecti (Hymenoptera: Eurytomidae), in French Polynesia and the Cook Islands. J. Med. Entomol. 52:1291–98
     [Google Scholar]
  99. 99.
    Martins A, Gallão J, Bichuette M, Santos E 2016. The first record of Notocyphus tyrannicus Smith, (Hymenoptera: Pompilidae) as parasitoid of Acanthoscurria ausserer, 1871 (Teraphosidae: Teraphosinae). Braz. J. Biol. 76:806–7
     [Google Scholar]
  100. 100.
    Matsumoto R. 2009.. “ Veils” against predators: modified web structure of a host spider induced by an ichneumonid parasitoid, Brachyzapus nikkoensis (Uchida) (Hymenoptera). J. Insect Behav. 22:39–48
     [Google Scholar]
  101. 101.
    Maure F, Brodeur J, Droit A, Doyon J, Thomas F. 2013. Bodyguard manipulation in a multipredator context: different processes, same effect. Behav. Process. 99:81–86
     [Google Scholar]
  102. 102.
    Maure F, Brodeur J, Ponlet N, Doyon J, Firlej A et al. 2011. The cost of a bodyguard. Biol. Lett. 7:843–46
     [Google Scholar]
  103. 103.
    Maure F, Doyon J, Thomas F, Brodeur J. 2014. Host behaviour manipulation as an evolutionary route towards attenuation of parasitoid virulence. J. Evol. Biol. 27:2871–75
     [Google Scholar]
  104. 104.
    Milbrath LR, Tauber MJ, Tauber CA. 1993. Prey specificity in Chrysopa: an interspecific comparison of larval feeding and defensive behavior. Ecology 74:1384–93
     [Google Scholar]
  105. 105.
    Mills N 2009. Parasitoids. Encyclopedia of Insects VH Resh, RT Cardé 748–51 San Diego: Academic. , 2nd ed..
     [Google Scholar]
  106. 106.
    Mizuno M, Itioka T, Tatematsu Y, Itô Y. 1997. Food utilization of aphidophagous hoverfly larvae (Diptera: Syrphidae, Chamaemyiidae) on herbaceous plants in an urban habitat. Ecol. Res. 12:239–48
     [Google Scholar]
  107. 107.
    Morse DH. 1994. The effect of host size on sex ratio in the ichneumonid wasp, Trychosis cyperia, a spider parasitoid. Am. Midl. Nat. 131:281–87
     [Google Scholar]
  108. 108.
    Nyffeler M, Birkhofer K. 2017. An estimated 400–800 million tons of prey are annually killed by the global spider community. Sci. Nat. 104:e30
     [Google Scholar]
  109. 109.
    Obrycki JJ, Tauber MJ, Tauber CA. 1985. Perilitus coccinellae (Hymenoptera: Braconidae): parasitization and development in relation to host-stage attacked. Ann. Entomol. Soc. Am. 78:852–54
     [Google Scholar]
  110. 110.
    Ode PJ, Vyas DK, Harvey JA. 2022. Extrinsic inter- and intra-specific competition in parasitoid wasps. Annu. Rev. Entomol. 67:305–28
     [Google Scholar]
  111. 111.
    Okuda T, Ceryngier P. 2000. Host discrimination in Dinocampus coccinellae (Hymenoptera: Braconidae), a solitary parasitoid of coccinellid beetles. Appl. Entomol. Zool. 35:535–39
     [Google Scholar]
  112. 112.
    Orr CJ, Obrycki JJ, Flanders RV. 1992. Host-acceptance behavior of Dinocampus coccinellae (Hymenoptera: Braconidae). Ann. Entomol. Soc. Am. 85:722–30
     [Google Scholar]
  113. 113.
    Orre GUS, Wratten SD, Jonsson M, Hale RJ. 2010. Effects of an herbivore-induced plant volatile on arthropods from three trophic levels in brassicas. Biol. Control 53:62–67
     [Google Scholar]
  114. 114.
    Owen CA, van Noort S, Compton SG, Coetzee JA. 2019. Nest site choice by the intertidal spider Desis formidabilis (Araneae: Desidae) and nest utilisation by its hymenopteran egg parasitoid. Ecol. Entomol. 44:62–70
     [Google Scholar]
  115. 115.
    Paula DP, Togni PH, Costa VA, Souza LM, Sousa AA et al. 2021. Scrutinizing the enemy release hypothesis: population effects of parasitoids on Harmonia axyridis and local host coccinellids in Brazil. BioControl 66:71–82
     [Google Scholar]
  116. 116.
    Pichersky E, Gershenzon J. 2002. The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr. Opin. Plant Biol. 5:237–43
     [Google Scholar]
  117. 117.
    Poelman EH, Cusumano A, de Boer JG. 2022. The ecology of hyperparasitoids. Annu. Rev. Entomol. 67:143–61
     [Google Scholar]
  118. 118.
    Poinar G. 2004. Behaviour and development of Elasmosoma sp. (Neoneurinae: Braconidae: Hymenoptera), an endoparasite of Formica ants (Formicidae: Hymenoptera). Parasitology 128:521–31
     [Google Scholar]
  119. 119.
    Quicke DLJ. 2014. The Braconid and Ichneumonid Parasitoid Wasps: Biology, Systematics, Evolution and Ecology Hoboken, NJ: Wiley
  120. 120.
    Rádai Z, Popovici O, Vas Z, Fusu L. 2018. First record of the parasitoid Idris flavicornis (Hymenoptera: Scelionidae) from eggs of the wolf spider Pardosa agrestis (Araneae: Lycosidae). Folia Entomol 79:101–6
     [Google Scholar]
  121. 121.
    Ramírez-Ahuja MDL, Garza-González E, Talamas EJ, Gómez-Govea MA, Rodríguez-Pérez MA et al. 2020. Parasitoids of Chrysopidae eggs in Sinaloa Mexico. Insects 11:e849
     [Google Scholar]
  122. 122.
    Reiss J, Bridle JR, Montoya JM, Woodward G. 2009. Emerging horizons in biodiversity and ecosystem functioning research. Trends Ecol. Evol. 24:505–14
     [Google Scholar]
  123. 123.
    Richerson JV, DeLoach CJ. 1972. Some aspects of host selection by Perilitus coccinellae. Ann. Entomol. Soc. Am. 65:834–39
     [Google Scholar]
  124. 124.
    Riechert SE, Lockley T. 1984. Spiders as biological control agents. Annu. Rev. Entomol. 29:299–320
     [Google Scholar]
  125. 125.
    Rivard I. 1964. Notes on parasitism of ground beetles (Coleoptera: Carabidae) in Ontario. Can. J. Zool. 42:919–20
     [Google Scholar]
  126. 126.
    Robinson KA. 2009. Use of floral resources by the lacewing Micromus tasmaniae and its parasitoid Anacharis zealandica, and the consequences for biological controlby M. tasmaniae. PhD Thesis Lincoln Univ. PA:
     [Google Scholar]
  127. 127.
    Romero V, Zaviezo T, Grez Villarroel A. 2020. The invasive coccinellid Harmonia axyridis (Coleoptera: Coccinellidae) is a less suitable host for parasitism than resident species. Cienc. Investig. Agrar. 47:312–23
     [Google Scholar]
  128. 128.
    Rotheray GE. 1984. Host relations, life cycles and multiparasitism in some parasitoids of aphidophagous Syrphidae (Diptera). Ecol. Entomol. 9:303–10
     [Google Scholar]
  129. 129.
    Schoonhoven LM, van Loon JJA, Dicke M. 2005. Insect-Plant Biology Oxford, UK: Oxford Univ. Press. , 2nd ed..
  130. 130.
    Scott EI. 1939. An account of the developmental stages of some aphidophagous Syrphidae (Dipt.) and their parasites (Hymenopt.). Ann. Appl. Biol. 26:509–32
     [Google Scholar]
  131. 131.
    Shuker DM, Pen I, Duncan AB, Reece SE, West SA 2005. Sex ratios under asymmetrical local mate competition: theory and a test with parasitoid wasps. Am. Nat. 166:301–16
     [Google Scholar]
  132. 132.
    Silva IMMS, Stouthamer R. 1999. Do sympatric Trichogramma species parasitize the pest insect Helicoverpa armigera and the beneficial insect Chrysoperla carnea in different proportions?. Entomol. Exp. Appl. 92:101–7
     [Google Scholar]
  133. 133.
    Sloggett JJ, Webberley KM, Majerus ME. 2004. Low parasitoid success on a myrmecophilous host is maintained in the absence of ants. Ecol. Entomol. 29:123–27
     [Google Scholar]
  134. 134.
    Sloggett JJ, Wood RA, Majerus ME. 1998. Adaptations of Coccinella magnifica Redtenbacher, a myrmecophilous coccinellid, to aggression by wood ants (Formica rufa group). I. Adult behavioral adaptation, its ecological context and evolution. J. Insect Behav. 11:889–904
     [Google Scholar]
  135. 135.
    Sluss R. 1968. Behavioral and anatomical responses of the convergent lady beetle to parasitism by Perilitus coccinellae (Schrank) (Hymenoptera: Braconidae). J. Invertebr. Pathol. 10:9–27
     [Google Scholar]
  136. 136.
    Smith HA, Chaney WE. 2007. A survey of syrphid predators of Nasonovia ribisnigri in organic lettuce on the central coast of California. J. Econ. Entomol. 100:39–48
     [Google Scholar]
  137. 137.
    Smith SM. 1996. Biological control with Trichogramma: advances, successes, and potential of their use. Annu. Rev. Entomol. 41:375–406
     [Google Scholar]
  138. 138.
    Soleimani S, Madadi H. 2015. Seasonal dynamics of: the pea aphid, Acyrthosiphon pisum (Harris), its natural enemies the seven spotted lady beetle Coccinella septempunctata Linnaeus and variegated lady beetle Hippodamia variegata Goeze, and their parasitoid Dinocampus coccinellae (Schrank). J Plant Prot. Res. 55:jppr–2015-0058
     [Google Scholar]
  139. 139.
    Song H, Meng L, Li B. 2017. Fitness consequences of body-size-dependent parasitism in a gregarious parasitoid attacking the 7-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae). Biol. Control 113:73–79
     [Google Scholar]
  140. 140.
    Stadler B, Dixon AFG. 2005. Ecology and evolution of aphid-ant interactions. Annu. Rev. Ecol. Evol. Sys. 36:345–72
     [Google Scholar]
  141. 141.
    Stanley E, Toscano-Gadea C, Aisenberg A. 2013. Spider hawk in sand dunes: Anoplius bicinctus (Hymenoptera: Pompilidae), a parasitoid wasp of the sex-role reversed spider Allocosa brasiliensis (Araneae: Lycosidae). J. Insect Behav. 26:514–24
     [Google Scholar]
  142. 142.
    Stelzl M, Devetak D. 1999. Neuroptera in agricultural ecosystems. Agric. Ecosyst. Environ. 74:305–21
     [Google Scholar]
  143. 143.
    Strand MR. 2014. Teratocytes and their functions in parasitoids. Curr. Opin. Insect Sci. 6:68–73
     [Google Scholar]
  144. 144.
    Sullivan DJ. 1987. Insect hyperparasitism. Annu. Rev. Entomol. 32:49–70
     [Google Scholar]
  145. 145.
    Sullivan DJ, Volkl W. 1999. Hyperparasitism: multitrophic ecology and behavior. Annu. Rev. Entomol. 44:291–315
     [Google Scholar]
  146. 146.
    Summers K, Speed M, Blount J, Stuckert A. 2015. Are aposematic signals honest? A review. J. Evol. Biol. 28:1583–99
     [Google Scholar]
  147. 147.
    Takasuka K, Fritzén NR, Tanaka Y, Matsumoto R, Maeto K, Shaw MR. 2018. The changing use of the ovipositor in host shifts by ichneumonid ectoparasitoids of spiders (Hymenoptera, Ichneumonidae, Pimplinae). Parasite 25:17
     [Google Scholar]
  148. 148.
    Takasuka K, Matsumoto R. 2011. Infanticide by a solitary koinobiont ichneumonid ectoparasitoid of spiders. Naturwissenschaften 98:529–36
     [Google Scholar]
  149. 149.
    Thiele H-U. 1977. Carabid Beetles in Their Environments: A Study on Habitat Selection by Adaptations in Physiology and Behaviour Berlin: Springer
  150. 150.
    Triltsch H. 1996. On the parasitization of the ladybird Coccinella septempunctata L. (Col., Coccinellidae). J. Appl. Entomol. 120:375–78
     [Google Scholar]
  151. 151.
    Trjapitzin VA, Shuvakhina EY. 2019. Contribution to the knowledge of the encyrtid-wasp genus Isodromus Howard, 1887 (Hymenoptera, Encyrtidae: Homalotylini), parasitoids of lacewings (Neuroptera, Chrysopidae) in the Palaearctic. Entomol. Rev. 99:1382–88
     [Google Scholar]
  152. 152.
    Turlings TCJ, Erb M. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: mechanisms, ecological relevance, and application potential. Annu. Rev. Entomol. 63:433–52
     [Google Scholar]
  153. 153.
    Turnbull A. 1973. Ecology of the true spiders (Araneomorphae). Annu. Rev. Entomol. 18:305–48
     [Google Scholar]
  154. 154.
    van Achterberg C. 1994. The Palaearctic species of the genus Chrysopophthorus Goidanich (Hymenoptera: Braconidae: Euphorinae). Zool. Meded. 68:301–7
     [Google Scholar]
  155. 155.
    van Baarlen P, Topping CJ, Sunderland KD. 1996. Host location by Gelis festinans, an eggsac parasitoid of the linyphiid spider Erigone atra. Entomol. Exp. Appl. 81:155–63
     [Google Scholar]
  156. 156.
    van Noort S, Masner L, Popovici O, Valerio AA, Taekul C et al. 2014. Systematics and biology of the aberrant intertidal parasitoid wasp Echthrodesis lamorali Masner (Hymenoptera: Platygastridae sl.): a parasitoid of spider eggs. Invertebr. Syst. 28:1–16
     [Google Scholar]
  157. 157.
    Vansant H, Vasquez YM, Obrycki JJ, Sethuraman A. 2019. Coccinellid host morphology dictates morphological diversity of the parasitoid wasp Dinocampus coccinellae. Biol. Control 133:110–16
     [Google Scholar]
  158. 158.
    Visser B, Le Lann C, Snaas H, Hardy IC, Harvey JA 2014. Consequences of resource competition for sex allocation and discriminative behaviors in a hyperparasitoid wasp. Behav. Ecol. Sociobiol. 68:105–13
     [Google Scholar]
  159. 159.
    Völkl W. 1995. Behavioral and morphological adaptations of the coccinellid, Platynaspis luteorubra for exploiting ant-attended resources (Coleoptera: Coccinellidae). J. Insect Behav. 8:653–70
     [Google Scholar]
  160. 160.
    Vosteen I, Gershenzon J, Kunert G. 2018. Dealing with food shortage: larval dispersal behaviour and survival on non-prey food of the hoverfly Episyrphus balteatus. Ecol. Entomol. 43:578–90
     [Google Scholar]
  161. 161.
    Vosteen I, Weisser WW, Kunert G. 2016. Is there any evidence that aphid alarm pheromones work as prey and host finding kairomones for natural enemies?. Ecol. Entomol. 41:1–12
     [Google Scholar]
  162. 162.
    Wang ZZ, Liu YQ, Shi M, Huang JH, Chen XX. 2019. Parasitoid wasps as effective biological control agents. J. Integr. Agric. 18:705–15
     [Google Scholar]
  163. 163.
    Way M, Khoo K. 1992. Role of ants in pest management. Annu. Rev. Entomol. 37:479–503
     [Google Scholar]
  164. 164.
    Weems HV. 1954. Natural enemies and insecticides that are detrimental to beneficial Syrphidae. Ohio J. Sci. 54:45–54
     [Google Scholar]
  165. 165.
    Weng JL, Barrantes G. 2007. Natural history and larval behavior of the parasitoid Zatypota petronae (Hymenoptera: Ichneumonidae). J. Hymenoptera Res. 16:326–35
     [Google Scholar]
  166. 166.
    Woodcock BA, Harrower C, Redhead J, Edwards M, Vanbergen AJ et al. 2014. National patterns of functional diversity and redundancy in predatory ground beetles and bees associated with key UK arable crops. J. Appl. Ecol. 51:142–51
     [Google Scholar]
  167. 167.
    Zang LS, Wang S, Zhang F, Desneux N. 2021. Biological control with Trichogramma in China: history, present status, and perspectives. Annu. Rev. Entomol. 66:463–84
     [Google Scholar]
/content/journals/10.1146/annurev-ento-120120-111607
Loading
The Biology and Ecology of Parasitoid Wasps of Predatory Arthropods
Annual Review of Entomology 68, 109 (2023); https://doi.org/10.1146/annurev-ento-120120-111607
/content/journals/10.1146/annurev-ento-120120-111607
/content/journals/10.1146/annurev-ento-120120-111607
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error