1932

Abstract

The main modes of action of insect parasitoids are considered to be killing their hosts with egg laying followed by offspring development (reproductive mortality), and adults feeding on hosts directly (host feeding). However, parasitoids can also negatively affect their hosts in ways that do not contribute to current or future parasitoid reproduction (nonreproductive effects). Outcomes of nonreproductive effects for hosts can include death, altered behavior, altered reproduction, and altered development. On the basis of these outcomes and the variety of associated mechanisms, we categorize nonreproductive effects into () nonconsumptive effects, () mutilation, () pseudoparasitism, () immune defense costs, and () aborted parasitism. These effects are widespread and can cause greater impacts on host populations than successful parasitism or host feeding. Nonreproductive effects constitute a hidden dimension of host–parasitoid trophic networks, with theoretical implications for community ecology as well as applied importance for the evaluation of ecosystem services provided by parasitoid biological control agents.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-011118-111753
2019-01-07
2024-06-15
Loading full text...

Full text loading...

/deliver/fulltext/ento/64/1/annurev-ento-011118-111753.html?itemId=/content/journals/10.1146/annurev-ento-011118-111753&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Abram PK, Brodeur J, Burte V, Boivin G 2016. Parasitoid-induced host egg abortion: an underappreciated component of biological control services provided by egg parasitoids. Biol. Control 98:52–60
    [Google Scholar]
  2. 2.  Abram PK, Gariepy TD, Boivin G, Brodeur J 2014. An invasive stink bug as an evolutionary trap for an indigenous egg parasitoid. Biol. Invas. 16:1387–95
    [Google Scholar]
  3. 3.  Asgari S, Rivers DB 2011. Venom proteins from endoparasitoid wasps and their role in host-parasite interactions. Annu. Rev. Entomol. 56:313–35
    [Google Scholar]
  4. 4.  Bannerman JA, Gillespie DR, Roitberg BD 2011. The impacts of extreme and fluctuating temperatures on trait-mediated indirect aphid–parasitoid interactions. Ecol. Entomol. 36:490–98
    [Google Scholar]
  5. 5.  Barnay O, Pizzol J, Gertz C, Kienlen JC, Hommay G, Lapchin L 1999. Host density-dependence of discovery and exploitation rates of egg patches of Lobesia botrana (Lepidoptera: Tortricidae) and Ephestia kuehniella (Lepidoptera: Pyralidae) by the parasitoid Trichogramma cacoeciae (Hymenoptera: Trichogrammatidae). J. Econ. Entomol. 92:1311–20
    [Google Scholar]
  6. 6.  Barrett BA, Brunner JF 1990. Types of parasitoid-induced mortality, host stage preferences, and sex ratios exhibited by Pnigalio flavipes (Hymenoptera: Eulophidae) using Phyllonorycter elmaella (Lepidoptera: Gracillariidae) as a host. Environ. Entomol. 19:803–7
    [Google Scholar]
  7. 7.  Barzman MS, Daane KM 2001. Host-handling behaviours in parasitoids of the black scale: a case for ant-mediated evolution. J. Anim. Ecol. 70:237–47
    [Google Scholar]
  8. 8.  Beckage NE, Gelman DB 2004. Wasp parasitoid disruption of host development: implications for new biologically based strategies for insect control. Annu. Rev. Entomol. 49:299–330Overview of the regulatory effects of parasitoid-injected compounds.
    [Google Scholar]
  9. 9.  Begg GS, Cook SM, Dye R, Ferrante M, Franck P et al. 2017. A functional overview of conservation biological control. Crop Prot 97:145–58
    [Google Scholar]
  10. 10.  Beltrà A, Soto A, Tena A 2015. How a slow-ovipositing parasitoid can succeed as a biological control agent of the invasive mealybug Phenacoccus peruvianus: implications for future classical and conservation biological control programs. BioControl 60:473–84
    [Google Scholar]
  11. 11.  Bernal JS, Luck RF, Morse JG, Drury MS 2001. Seasonal and scale size relationships between citricola scale (Homoptera: Coccidae) and its parasitoid complex (Hymenoptera: Chalcidoidea) on San Joaquin Valley citrus. Biol. Control 20:210–21
    [Google Scholar]
  12. 12.  Blumberg D 1997. Parasitoid encapsulation as a defense mechanism in the Coccoidea (Homoptera) and its importance in biological control. Biol. Control 8:225–36
    [Google Scholar]
  13. 13.  Boisseau RP, Woods HA, Goubault M 2017. The metabolic costs of fighting and host exploitation in a seed-drilling parasitic wasp. J. Exp. Biol. 220:3955–66
    [Google Scholar]
  14. 14.  Brodeur J, Rosenheim JA 2000. Intraguild interactions in aphid parasitoids. Entomol. Exp. Appl. 97:93–108
    [Google Scholar]
  15. 15.  Brown JJ, Kainoh Y 1992. Host castration by Ascogaster spp. (Hymenoptera: Braconidae). Ann. Entomol. Soc. Am. 85:67–71
    [Google Scholar]
  16. 16.  Campbell RW 1963. Some ichneumonid-sarcophagid interactions in the gypsy moth Porthetria dispar (L.) (Lepidoptera: Lymantriidae). Can. Entomol. 95:337–45
    [Google Scholar]
  17. 17.  Carton Y, David JR 1983. Reduction of fitness in Drosophila adults surviving parasitization by a cynipid wasp. Experientia 39:231–33
    [Google Scholar]
  18. 18.  Carton Y, Kitano H 1981. Evolutionary relationships to parasitism by seven species of the Drosophila melanogaster subgroup. Biol. J. Linn. Soc. 16:227–41
    [Google Scholar]
  19. 19.  Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG 2013. Complex cocktails: the evolutionary novelty of venoms. Trends Ecol. Evolut. 28:219–29
    [Google Scholar]
  20. 20.  Cebolla R, Vanaclocha P, Urbaneja A, Tena A 2018. Overstinging by hymenopteran parasitoids causes mutilation and surplus killing of hosts. J. Pest Sci. 91:327–39Thoroughly measures magnitude and condition dependence of mutilation/pseudoparasitism.
    [Google Scholar]
  21. 21.  Charles JG, Sandanayaka WM, Chhagan A, Page-Weir NE 2013. Survival of the gregarious ectoparasitoid Mastrus ridens on codling moth, Cydia pomonella, and non-target species. BioControl 58:505–13
    [Google Scholar]
  22. 22.  Chau A, Mackauer M 1997. Dropping of pea aphids from feeding site: a consequence of parasitism by the wasp, Monoctonus paulensis. Entomol. Exp. Appl. 83:247–52
    [Google Scholar]
  23. 23.  Condon MA, Scheffer SJ, Lewis ML, Wharton R, Adams DC, Forbes AA 2014. Lethal interactions between parasites and prey increase niche diversity in a tropical community. Science 343:1240–44
    [Google Scholar]
  24. 24.  Coudron TA, Kelly TJ, Puttler B 1990. Developmental responses of Trichoplusia ni (Lepidoptera: Noctuidae) to parasitism by the ectoparasite Euplectrus plathypenae (Hymenoptera: Eulophidae). Arch. Insect Biochem. Physiol. 13:83–94
    [Google Scholar]
  25. 25.  de Bach P 1943. The importance of host-feeding by adult parasites in the reduction of host populations. J. Econ. Entomol. 36:647–58
    [Google Scholar]
  26. 26.  Deas JB, Hunter MS 2012. Mothers modify eggs into shields to protect offspring from parasitism. Proc. R. Soc. B. 279:847–53Demonstrates a nonconsumptive effect of an egg parasitoid on egg-laying adults of their hosts.
    [Google Scholar]
  27. 27.  Deas JB, Hunter MS 2013. Delay, avoidance and protection in oviposition behaviour in response to fine-scale variation in egg parasitism risk. Anim. Behav. 86:933–40
    [Google Scholar]
  28. 28.  Desneux N, Barta RJ, Hoelmer KA, Hopper KR, Heimpel GE 2009. Multifaceted determinants of host specificity in an aphid parasitoid. Oecologia 160:387–98
    [Google Scholar]
  29. 29.  Dill LM, Fraser AH, Roitberg BD 1990. The economics of escape behaviour in the pea aphid, Acyrthosiphon pisum. Oecologia 83:473–78
    [Google Scholar]
  30. 30.  Duan JJ, Watt TJ, Larson K 2014. Biology, life history, and laboratory rearing of Spathius galinae (Hymenoptera: Braconidae), a larval parasitoid of the invasive emerald ash borer (Coleoptera: Buprestidae). J. Econ. Entomol. 107:939–46
    [Google Scholar]
  31. 31.  Duodu YA, Davis DW 1974. Selection of alfalfa weevil larval instars by, and mortality due to, the parasite Bathyplectes curculionis (Thomson). Environ. Entomol. 3:549–52
    [Google Scholar]
  32. 32.  Eliopoulos PA, Kapranas A, Givropoulou EG, Hardy ICW 2017. Reproductive efficiency of the bethylid wasp Cephalonomia tarsalis: the influences of spatial structure and host density. Bull. Entomol. Res. 107:139–47
    [Google Scholar]
  33. 33.  Fellowes MDE, Kraaijeveld AR, Godfray HCJ 1999. The relative fitness of Drosophila melanogaster (Diptera, Drosophilidae) that have successfully defended themselves against the parisitoid Asobara tabida (Hymenoptera, Braconidae). J. Evolut. Biol. 12:123–28
    [Google Scholar]
  34. 34.  Fellowes MDE, Masnatta P, Kraaijeveld AR, Godfray HCJ 1998. Pupal parasitoid attack influences the relative fitness of Drosophila that have encapsulated larval parasitoids. Ecol. Entomol. 23:281–84
    [Google Scholar]
  35. 35.  Fill A, Long EY, Finke DL 2012. Non-consumptive effects of a natural enemy on a non-prey herbivore population. Ecol. Entomol. 37:43–50
    [Google Scholar]
  36. 36.  Flanders SE 1953. Predatism by the adult hymenopterous parasite and its role in biological control. J. Econ. Entomol. 46:541–44
    [Google Scholar]
  37. 37.  Gariepy TD, Kuhlmann U, Gillott C, Erlandson M 2008. A large-scale comparison of conventional and molecular methods for the evaluation of host–parasitoid associations in non-target risk-assessment studies. J. Appl. Ecol. 45:708–15
    [Google Scholar]
  38. 38.  Geden CJ, Moon RD 2009. Host ranges of gregarious muscoid fly parasitoids: Muscidifurax raptorellus (Hymenoptera: Pteromalidae), Tachinaephagus zealandicus (Hymenoptera: Encyrtidae), and Trichopria nigra (Hymenoptera: Diapriidae). Environ. Entomol. 38:700–7
    [Google Scholar]
  39. 39.  Godfray HCJ 1994. Parasitoids: Behavioral and Evolutionary Ecology Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  40. 40.  Godwin PA, Odell TM 1984. Laboratory study of competition between Blepharipa pratensis and Parasetigena silvestris (Diptera: Tachinidae) in Lymantria dispar (Lepidoptera: Lymantriidae). Environ. Entomol. 13:1059–63
    [Google Scholar]
  41. 41.  Goldson SL, Proffitt JR, McNeill MR, Phillips CB, Barlow ND, Baird DB 2004. Unexpected Listronotus bonariensis (Coleoptera: Curculionidae) mortality in the presence of parasitoids. Bull. Entomol. Res. 94:411–17
    [Google Scholar]
  42. 42.  Gowling GR, van Emden HV 1994. Falling aphids enhance impact of biological control by parasitoids on partially aphid-resistant plant varieties. Ann. Appl. Biol. 125:233–42
    [Google Scholar]
  43. 43.  Guzo D, Stoltz DB 1985. Obligatory multiparasitism in the tussock moth, Orgyia leucostigma. Parasitology 90:1–10
    [Google Scholar]
  44. 44.  Hawkins BA, Sheehan W 1994. Parasitoid Community Ecology Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  45. 45.  Heimpel GE, Mills NJ 2017. Biological Control: Ecology and Applications Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  46. 46.  Heimpel GE, Neuhauser C, Hoogendoorn M 2003. Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid. Ecol. Lett. 6:556–66
    [Google Scholar]
  47. 47.  Heinz KM, Parrella MP 1989. Attack behavior and host size selection by Diglyphus begini on Liriomyza trifolii in chrysanthemum. Entomol. Exp. Appl. 53:147–56
    [Google Scholar]
  48. 48.  Hermann SL, Landis DA 2017. Scaling up our understanding of non-consumptive effects in insect systems. Curr. Opin. Insect Sci. 20:54–60
    [Google Scholar]
  49. 49.  Hoang A 2001. Immune response to parasitism reduces resistance of Drosophila melanogaster to desiccation and starvation. Evolution 55:2353–58Examines interactive effects of adverse environmental conditions and costly host immune response.
    [Google Scholar]
  50. 50.  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]
  51. 51.  Huang J, Hua H-Q, Wang L-Y, Zhang F, Li Y-X 2017. Number of attacks by Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae) affects the successful parasitism of Ostrinia furnacalis (Lepidoptera: Crambidae) eggs. Bull. Entomol. Res. 107:812–19
    [Google Scholar]
  52. 52.  Ingerslew KS, Finke DL 2017. Mechanisms underlying the nonconsumptive effects of parasitoid wasps on aphids. Environ. Entomol. 46:75–83
    [Google Scholar]
  53. 53.  Islam KS, Perera HAS, Copland MJW 1997. The effects of parasitism by an encyrtid parasitoid, Anagyrus pseudococci on the survival, reproduction and physiological changes of the mealybug, Planococcus citri. Entomol. Exp. Appl. 84:77–83
    [Google Scholar]
  54. 54.  Jervis MA, Kidd NAC 1986. Host-feeding strategies in hymenopteran parasitoids. Biol. Rev. 61:395–434
    [Google Scholar]
  55. 55.  Jones D 1986. Chelonus sp.: suppression of host ecdysteroids and developmentally stationary pseudoparasitized prepupae. Exp. Parasitol. 61:10–17
    [Google Scholar]
  56. 56.  Jones D, Jones G, Hammock BD 1981. Developmental and behavioural responses of larval Trichoplusia ni to parasitization by an imported braconid parasite Chelonus sp. Physiol. Entomol. 6:387–94
    [Google Scholar]
  57. 57.  Jones D, Jones G, Rudnicka M, Click A, Reck-Malleczewen V, Iwaya M 1986. Pseudoparasitism of host Trichoplusia ni by Chelonus spp. as a new model system for parasite regulation of host physiology. J. Insect Physiol. 32:315–19, 321–28
    [Google Scholar]
  58. 58.  Jones TS, Bilton AR, Mak L, Sait SM 2015. Host switching in a generalist parasitoid: contrasting transient and transgenerational costs associated with novel and original host species. Ecol. Evolut. 5:459–65
    [Google Scholar]
  59. 59.  Kaser JM, Heimpel GE 2015. Linking risk and efficacy in biological control host–parasitoid models. Biol. Control 90:49–60
    [Google Scholar]
  60. 60.  Kaser JM, Nielsen AL, Abram PK 2018. Biological control effects of non-reproductive host mortality caused by insect parasitoids. Ecol. Appl. 28:1081–92First modeling study of indirect ecological consequences of nonreproductive effects.
    [Google Scholar]
  61. 61.  Kaspi R, Yuval B, Parrella MP 2011. Anticipated host availability increases parasitoid host attack behaviour. Anim. Behav. 82:1159–65
    [Google Scholar]
  62. 62.  Keinan Y, Kishinevsky M, Segoli M, Keasar T 2012. Repeated probing of hosts: an important component of superparasitism. Behav. Ecol. 23:1263–68
    [Google Scholar]
  63. 63.  Kraaijeveld AR, Godfray HCJ 1997. Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389:278–80
    [Google Scholar]
  64. 64.  Lashomb J, Krainacker D, Jansson RK, Ng YS, Chianese R 1987. Parasitism of Leptinotarsa decemlineata (Say) eggs by Edovum puttleri Grissell (Hymenoptera: Eulophidae): effects of host age, parasitoid age, and temperature. Can. Entomol. 119:75–82
    [Google Scholar]
  65. 65.  Legner EF 1979. The relationship between host destruction and parasite reproductive potential in Muscidifurax raptor, M. zaraptor, and Spalangia endius [Chalcidoidea: Pteromalidae]. BioControl 24:145–52
    [Google Scholar]
  66. 66.  Legner EF 1988. Quantitation of heterotic behavior in parasitic Hymenoptera. Ann. Entomol. Soc. Am. 81:657–81
    [Google Scholar]
  67. 67.  Liu W-X, Wang W-X, Zhang Y-B, Wang W, Lu S-L, Wan F-H 2015. Adult diet affects the life history and host-killing behavior of a host-feeding parasitoid. Biol. Control 81:58–64
    [Google Scholar]
  68. 68.  Lynch ZR, Schlenke TA, Roode JC 2016. Evolution of behavioural and cellular defences against parasitoid wasps in the Drosophila melanogaster subgroup. J. Evol. Biol. 29:1016–29
    [Google Scholar]
  69. 69.  Lysyk TJ 2004. Host mortality and progeny production by solitary and gregarious parasitoids (Hymenoptera: Pteromalidae) attacking Musca domestica and Stomoxys calcitrans (Diptera: Muscidae) at varying host densities. Environ. Entomol. 33:328–39
    [Google Scholar]
  70. 70.  Mandeville JD, Mullens BA 1990. Host preference and learning in Muscidifurax zaraptor (Hymenoptera: Pteromalidae). Ann. Entomol. Soc. Am. 83:1203–9
    [Google Scholar]
  71. 71.  Martinez-Ferrer MT, Grafton-Cardwell EE, Shorey HH 2003. Disruption of parasitism of the California red scale (Homoptera: Diaspididae) by three ant species (Hymenoptera: Formicidae). Biol. Control 26:279–86
    [Google Scholar]
  72. 72.  McGonigle JE, Leitão AB, Ommeslag S, Smith S, Day JP, Jiggins FM 2017. Parallel and costly changes to cellular immunity underlie the evolution of parasitoid resistance in three Drosophila species. PLOS Pathog 13:e1006683
    [Google Scholar]
  73. 73.  Minot MC, Leonard DE 1976. Host preference and development of the parasitoid Brachymeria intermedia in Lymantria dispar, Galleria mellonella, and Choristoneura fumiferana. Environ. Entomol. 5:527–32
    [Google Scholar]
  74. 74.  Münster-Swendsen M 1994. Pseudoparasitism: detection and ecological significance in Epinotia tedella (Cl.) (Tortricidae). Nor. J. Agric. Sci. Suppl. 16:329–35
    [Google Scholar]
  75. 75.  Münster-Swendsen M 2002. Population cycles of the spruce needleminer in Denmark driven by interactions with insect parasitoids. Population Cycles: The Case for Trophic Interactions A Berryman 29–43 Oxford, UK: Oxford Univ. PressHighlights the importance of nonreproductive effects on host–parasitoid population cycles.
    [Google Scholar]
  76. 76.  Münster-Swendsen M, Berryman A 2005. Detecting the causes of population cycles by analysis of R-functions: the spruce needleminer, Epinotia tedella, and its parasitoids in Danish spruce plantations. Oikos 108:495–502
    [Google Scholar]
  77. 77.  Niogret J, Sait SM, Rohani P 2009. Parasitism and constitutive defence costs to host life-history traits in a parasitoid–host interaction. Ecol. Entomol. 34:763–71
    [Google Scholar]
  78. 78.  Neuenschwander P, Madojemu E 1986. Mortality of the cassava mealybug, Phenacoccus manihoti Mat.-Ferr.(Hom., Pseudococcidae), associated with an attack by Epidinocarsis lopezi (Hym., Encyrtidae). Mitt. Schweiz. Entomol. 59:57–62Implicates nonreproductive effects impacts in success of a classical biological control agent.
    [Google Scholar]
  79. 79.  Ode PJ, Rosenheim JA 1998. Sex allocation and the evolutionary transition between solitary and gregarious parasitoid development. Am. Nat. 152:757–61
    [Google Scholar]
  80. 80.  Ohno K 1987. Effect of host age on parasitism by Trissolcus plautiae (Watanabe) (Hymenoptera: Scelionidae), an egg parasitoid of Plautia stali Scott (Heteroptera: Pentatomidae). Appl. Entomol. Zool. 22:646–48
    [Google Scholar]
  81. 81.  Parvizi Y, Rasekh A, Michaud JP 2018. Cornicle secretions by Aphis fabae (Hemiptera: Aphididae) result in age-dependent costs and improved host suitability for Lysiphlebus fabarum (Marshall) (Hymenoptera: Braconidae). Bull. Entomol. Res. 108:685–93
    [Google Scholar]
  82. 82.  Patel KJ, Schuster DJ 1991. Temperature-dependent fecundity, longevity, and host-killing activity of Diglyphus intermedius (Hymenoptera: Eulophidae) on third instars of Liriomyza trifolii (Burgess) (Diptera: Agromyzidae). Environ. Entomol. 20:1195–99
    [Google Scholar]
  83. 83.  Patel KJ, Schuster DJ, Smerage GH 2003. Density dependent parasitism and host-killing of Liriomyza trifolii (Diptera: Agromyzidae) by Diglyphus intermedius (Hymenoptera: Eulophidae). Fla. Entomol. 86:8–14
    [Google Scholar]
  84. 84.  Pawson BM, Petersen JJ 1988. Dispersal of Muscidifurax zaraptor (Hymenoptera: Pteromalidae), a filth fly parasitoid, at dairies in eastern Nebraska. Environ. Entomol. 17:398–402
    [Google Scholar]
  85. 85.  Picard C, Auclair JL, Boivin G 1991. Response to host age of the egg parasitoid Anaphes n.sp. (Hymenoptera: Mymaridae). Biocontrol Sci. Tech. 1:169–76
    [Google Scholar]
  86. 86.  Pimentel D, Levin SA, Olson D 1978. Coevolution and the stability of exploiter-victim systems. Am. Nat. 112:119–25
    [Google Scholar]
  87. 87.  Pizzol J, Desneux N, Wajnberg E, Thiéry D 2012. Parasitoid and host egg ages have independent impact on various biological traits in a Trichogramma species. J. Pest Sci. 85:489–96
    [Google Scholar]
  88. 88.  Poulin R 2011. The many roads to parasitism: a tale of convergence. Advances in Parasitology 74 D Rollinson, SI Hay London: Academic
    [Google Scholar]
  89. 89.  Preisser EL, Bolnick DI 2008. The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLOS ONE 3:e2465
    [Google Scholar]
  90. 90.  Price PW 1980. Evolutionary Biology of Parasites Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  91. 91.  Quednau FW 1970. Notes on life-history, fecundity, longevity, and attack pattern of Agathis pumila (Hymenoptera: Braconidae), a parasite of the larch casebearer. Can. Entomol. 102:736–45
    [Google Scholar]
  92. 92.  Rahman M 1970. Mutilation of the imported cabbageworm by the parasite Apanteles rubecula. J. Econ. Entomol. 63:1114–16
    [Google Scholar]
  93. 93.  Reed-Larsen DA, Brown JJ 1990. Embryonic castration of the codling moth, Cydia pomonella by an endoparasitoid, Ascogaster quadridentata. J. Insect Physiol. 36:111–18
    [Google Scholar]
  94. 94.  Rivers DB, Ruggiero L, Hayes M 2002. The ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) differentially affects cells mediating the immune response of its flesh fly host, Sarcophaga bullata Parker (Diptera: Sarcophagidae). J. Insect Physiol. 48:1053–64
    [Google Scholar]
  95. 95.  Roitberg BD, Myers JH 1979. Behavioural and physiological adaptations of pea aphids (Homoptera: Aphididae) to high ground temperatures and predator disturbance. Can. Entomol. 111:515–19
    [Google Scholar]
  96. 96.  Rosenheim JA 1999. The relative contributions of time and eggs to the cost of reproduction. Evolution 53:376–85
    [Google Scholar]
  97. 97.  Ryan RB 1985. Relationship between parasitism of larch casebearer (Lepidoptera: Coleophoridae) and dead hosts in the Blue Mountains, 1973–1983. Can. Entomol. 117:935–39
    [Google Scholar]
  98. 98.  Salt G 1968. The resistance of insect parasitoids to the defence reactions of their hosts. Biol. Rev. 43:200–32
    [Google Scholar]
  99. 99.  Schlaepfer MA, Sherman PW, Blossey B, Runge MC 2005. Introduced species as evolutionary traps. Ecol. Lett. 8:241–46
    [Google Scholar]
  100. 100.  Sinha TB, Singh R 1980. Bionomics of Trioxys (Binodoxys) indicus, an aphidiid parasitoid of Aphis craccivora. III. Numerical aspects of the interaction of the parasitoid and its host. Entomol. Exp. Appl. 28:167–76
    [Google Scholar]
  101. 101.  Sloggett JJ, Weisser WW 2002. Parasitoids induce production of the dispersal morph of the pea aphid, Acyrthosiphon pisum. Oikos 98:323–33First to demonstrate an indirect influence of parasitoids on insect polyphenism (altered development).
    [Google Scholar]
  102. 102.  Spence JR 1986. Interactions between the scelionid egg parasitoid Tiphodytes gerriphagus (Hymenoptera) and its gerrid hosts (Heteroptera). Can. J. Zool. 64:2728–38
    [Google Scholar]
  103. 103.  Sterk G, Hassan SA, Baillod M, Bakker F, Bigler F et al. 1999. Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working Group ‘Pesticides and Beneficial Organisms’. BioControl 44:99–117
    [Google Scholar]
  104. 104.  Stireman JO, Nason JD, Heard SB, Seehawer JM 2006. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc. R. Soc. B 273:523–30
    [Google Scholar]
  105. 105.  Strand MR 2014. Teratocytes and their functions in parasitoids. Curr. Opin. Insect Sci. 6:68–73
    [Google Scholar]
  106. 106.  Strand MR, Meola SM, Vinson SB 1986. Correlating pathological symptoms in Heliothis virescens eggs with development of the parasitoid Telenomus heliothidis. J. Insect Physiol 32:389–402
    [Google Scholar]
  107. 107.  Strand MR, Pech LL 1995. Immunological basis for compatibility in parasitoid-host relationships. Annu. Rev. Entomol. 40:31–56
    [Google Scholar]
  108. 108.  Strand MR, Ratner S, Vinson SB 1983. Maternally induced host regulation by the egg parasitoid Telenomus heliothidis. Physiol. Entomol 8:469–75
    [Google Scholar]
  109. 109.  Tamaki G, Halfhill JE, Hathaway DO 1970. Dispersal and reduction of colonies of pea aphids by Aphidius smithi (Hymenoptera: Aphidiidae). Ann. Entomol. Soc. Am. 63:973–80First report of nonconsumptive effects of parasitoids on aphids.
    [Google Scholar]
  110. 110.  Tang L-D, Ji X-C, Han Y, Fu B-L, Liu K 2015. Parasitism, emergence, and development of Spalangia endius (Hymenoptera: Pteromalidae) in pupae of different ages of Bactrocera cucurbitae (Diptera: Tephritidae). J. Insect Sci. 15:15
    [Google Scholar]
  111. 111.  Tena A, Beltrà A, Soto A 2012. Novel defenses of Protopulvinaria pyriformis (Hemiptera: Coccidea) against its major parasitoid Metaphycus helvolus (Hymenoptera: Encyrtidae): implications for biological control of soft scales. Biol. Control 62:45–52
    [Google Scholar]
  112. 112.  Tena A, Kapranas A, Garcia-Marí F, Luck RF 2008. Host discrimination, superparasitism and infanticide by a gregarious endoparasitoid. Anim. Behav. 76:789–99
    [Google Scholar]
  113. 113.  Thorpe KW, Raupp MJ, Odell TM 1990. Assessing gypsy moth (Lepidoptera: Lymantriidae) larval mortality caused by the parasitoid Cotesia melanoscela (Hymenoptera: Braconidae): host age effects. Environ. Entomol. 19:771–75
    [Google Scholar]
  114. 114.  Tillinger NA, Hoch G, Schopf A 2004. Effects of parasitoid associated factors of the endoparasitoid Glyptapanteles liparidis (Hymenoptera: Braconidae). Eur. J. Entomol. 101:243–50
    [Google Scholar]
  115. 115.  van Alphen JJM, Visser ME 1990. Superparasitism as an adaptive strategy for insect parasitoids. Annu. Rev. Entomol. 35:59–79
    [Google Scholar]
  116. 116.  Van Driesche RG 1983. Meaning of “percent parasitism” in studies of insect parasitoids. Environ. Entomol. 12:1611–22
    [Google Scholar]
  117. 117.  Van Driesche RG, Bellotti AC, Castillo J, Herrera CJ 1990. Estimating total losses from parasitoids for a field population of a continuously breeding insect, cassava mealybug, Phenacoccus herreni (Homoptera: Pseudococcidae) in Colombia, SA. Fla. Entomol. 73:133–43Applies correction from laboratory estimates of nonreproductive effects in the field.
    [Google Scholar]
  118. 118.  Van Driesche RG, Bellotti AC, Herrera CJ, Castello JA 1987. Host feeding and ovipositor insertion as sources of mortality in the mealybug Phenacoccus herreni caused by two encyrtids, Epidinocarsis diversicornis and Acerophagus coccois. Entomol. Exp. Appl. 44:97–100
    [Google Scholar]
  119. 119.  Vásquez LA, Shelton AM, Hoffmann MP, Roush RT 1997. Laboratory evaluation of commercial Trichogrammatid products for potential use against Plutella xylostella (L.) (Lepidoptera: Plutellidae). Biol. Control 9:143–48
    [Google Scholar]
  120. 120.  Vereijssen J, Armstrong KF, Barratt BI, Crawford AM, McNeill M, Goldson SL 2011. Evidence for parasitoid-induced premature mortality in the Argentine stem weevil. Physiol. Entomol. 36:194–99
    [Google Scholar]
  121. 121.  Vet LEM, Dicke M 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37:141–72
    [Google Scholar]
  122. 122.  Vinson SB 1976. Host selection by insect parasitoids. Annu. Rev. Entomol. 21:109–33
    [Google Scholar]
  123. 123.  Vinson SB, Iwantsch GF 1980. Host regulation by insect parasitoids. Q. Rev. Biol. 55:143–65
    [Google Scholar]
  124. 124.  Zhang Y-b, Liu W-x, Wang W, Wan F-h, Li Q 2011. Lifetime gains and patterns of accumulation and mobilization of nutrients in females of the synovigenic parasitoid, Diglyphus isaea Walker (Hymenoptera: Eulophidae), as a function of diet. J. Insect Physiol. 57:1045–52
    [Google Scholar]
/content/journals/10.1146/annurev-ento-011118-111753
Loading
/content/journals/10.1146/annurev-ento-011118-111753
Loading

Data & Media loading...

  • Article Type: Review Article
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