The number of parasitoids developed per host is one of the major factors that influences future adult body size and reproductive success. Here, we examined four external factors (host species, heritability, host population density, and presence of predators) that can affect the number of the gregarious parasitoid Anaphes flavipes (Förster, 1841) (Hymenoptera: Mymaridae) wasps developing in one host. The effect of host population density on the number of parasitoid offspring developed per host was confirmed, and for the first time, we also showed that the number of offspring per host is influenced by the presence of predators. Low host density and presence of predators increases the number of wasps developed in one host egg. However, a higher number of A. flavipes in one host reduces A. flavipes body size and hence its future individual fertility and fitness. Our results highlighted the importance of some external factors that distinctly affect the number of wasp offspring. Therefore, in this context, we suggest that in comparison to solitary parasitoids, the gregarious parasitoid A. flavipes can better respond to various external factors and can more flexibly change its population density.

Crop Research Institute Drnovská 507 CZ 161 06 Praha 6 Ruzyně Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 CZ 128 43 Praha 2 Czech Republic

Institute of Entomology Biological Centre Czech Academy of Sciences Branišovská 31 CZ 370 05 České Budějovice Czech Republic

Zobrazit více v PubMed

Mayhew PJ, van Alphen JJM. Gregarious development in alysiine parasitoids evolved through a reduction in larval aggression. Anim. Behav. 1999;58:131–141. doi: 10.1006/anbe.1999.1106. PubMed DOI

Schmidt JM, Smith JJB. Correlations between body angles and substrate curvature in the parasitoid wasp Trichogramma minutum: a possible mechanism of host radius measurement. J. Exp. Biol. 1986;125:271–285.

Rosenheim JA, Wilhoit LR, Armer CA. Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia. 1993;96:439–449. doi: 10.1007/BF00317517. PubMed DOI

Mayhew PJ. The evolution of gregariousness in parasitoid wasps. P. Roy. Soc. Lond. B. Bio. 1998;265:383–389. doi: 10.1098/rspb.1998.0306. DOI

Klomp H, Teerink BJ. Host selection and number of eggs per oviposition in the egg parasite Trichgramma embryophagum Htg. Nature. 1962;195:1020–1021. doi: 10.1038/1951020a0. DOI

Van Alphen JJM, Drijver RAB. Host selection by Asobara tabida Nees (Braconidae: Alysiinae), a larval parasitoid of fruit inhabiting Drosophila species. I. Host stage selection with Drosophila melanogaster as host. Neth. J. Zool. 1982;32:215–231.

Koppik M, Thiel A, Hoffmeister TS. Adaptive decision making or differential mortality: what causes offspring emergence in a gregarious parasitoid? Entomol. Exp. Appl. 2014;150:208–216. doi: 10.1111/eea.12154. DOI

Waage JK, Lane JA. The reproductive strategy of a parasitic wasp: II. Sex allocation and local mate competition in Trichogramma evanescens. J. Anim. Ecol. 1984;53:417–426. doi: 10.2307/4525. DOI

King BH. Offspring sex ratios in parasitoid wasps. Q. Rev. Biol. 1987;62:367–396. doi: 10.1086/415618. DOI

King BH. Host-size-dependent sex ratios among parasitoid wasps: does host growth matter? Oecologia. 1989;78:420–426. doi: 10.1007/BF00379119. PubMed DOI

Godfray, H. C. J. 1994. Parasitoids: behavioral and evolutionary ecology. (Princeton University Press, 1994).

Bai B, Luck RF, Forster L, Stephens B, Janssen JM. The effect of host size on quality attributes of the egg parasitoid, Trichogramma pretiosum. Entomol. Exp. Appl. 1992;64:37–48. doi: 10.1111/j.1570-7458.1992.tb01592.x. DOI

Kazmer DJ, Luck RF. Field Tests of the Size‐Fitness Hypothesis in the Egg Parasitoid Trichogramma Pretiosum. Ecology. 1995;76:412–425. doi: 10.2307/1941200. DOI

Klomp H, Teerink BJ. The elimination of supernumerary larvae of the gregarious egg-parasitoid Trichogramma embryophagum [Hym.: Trichogrammatidae] in eggs of the host Ephestia kuehniella [Lep.: Pyralidae] Biocontrol. 1978;23:153–159.

Carbone S, Nieto MP, Rivera AC. Maternal size and age affect offspring sex ratio in the solitary egg parasitoid Anaphes nitens. Entomol. Exp. Appl. 2007;125:23–32. doi: 10.1111/j.1570-7458.2007.00595.x. DOI

Mayhew PJ. Offspring size-number strategy in the bethylid parasitoid Laelius pedatus. Behav. Ecol. 1998;9:54–59. doi: 10.1093/beheco/9.1.54. DOI

Cloutier C, Duperron J, Tertuliano M, McNeil JN. Host instar, body size and fitness in the koinobiotic parasitoid Aphidius nigripes. Entomol. Exp. Appl. 2000;97:29–40. doi: 10.1046/j.1570-7458.2000.00713.x. DOI

Gao SK, Wei K, Tang YL, Wang XY, Yang ZQ. Effect of parasitoid density on the timing of parasitism and development duration of progeny in Sclerodermus pupariae (Hymenoptera: Bethylidae) Biol. Control. 2016;97:57–62. doi: 10.1016/j.biocontrol.2016.03.003. DOI

Klomp H, Teerink BJ. The significance of oviposition rates in the egg parasite, Trichogramma embryophagum Htg. Arch. Neerl. Zool. 1967;17:350–375. doi: 10.1163/036551667X00065. DOI

Bezemer TM, Mills NJ. Clutch size decisions of a gregarious parasitoid under laboratory and field conditions. Anim. Behav. 2003;66:1119–1128. doi: 10.1006/anbe.2003.2296. DOI

Zaviezo T, Mills N. Factors influencing the evolution of clutch size in a gregarious insect parasitoid. J. Anim. Ecol. 2000;69:1047–1057. doi: 10.1046/j.1365-2656.2000.00460.x. DOI

Clutton-Brock TH. Sex ratio variation in birds. Ibis. 1986;128:317–329. doi: 10.1111/j.1474-919X.1986.tb02682.x. DOI

Hardy IC. Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos. 1994;69:3–20. doi: 10.2307/3545278. DOI

Mayhew PJ, Godfray HCJ. Mixed sex allocation strategies in a parasitoid wasp. Oecologia. 1997;110:218–221. doi: 10.1007/s004420050153. PubMed DOI

Anderson RC, Paschke JD. The biology and ecology of Anaphes flavipes (Hymenoptera: Mymaridae), an exotic egg parasite of the cereal leaf beetle. Ann. Entomol. Soc. Am. 1968;61:1–5. doi: 10.1093/aesa/61.1.1. DOI

Waage JK, Ming NS. The reproductive strategy of a parasitic wasp: I. optimal progeny and sex allocation in Trichogramma evanescens. J. Anim. Ecol. 1984;53:401–415. doi: 10.2307/4524. DOI

Samková A, Janšta P, Huber TJ. Anaphes flavipes (Foester, 1841) redescription, neotype designation, and comparison with A. nipponicus Kuwayama, 1932 (Hymenoptera: Chalcidoidea: Mymaridae) Acta Ent. Mus. Nat. Pra. 2017;57:677–711.

Samková A, Hadrava J, Skuhrovec J, Janšta P. Reproductive strategy as a major factor determining female body size and fertility of a gregarious parasitoid. J. Appl. Entomol. 2019 doi: 10.1111/jen.12615. DOI

Sequeira R, Mackauer M. Nutritional Ecology of an Insect Host‐Parasitoid Association: The Pea Aphid‐Aphidius Ervi System. Ecology. 1992;73:183–189. doi: 10.2307/1938730. DOI

Elzinga JA, Harvey JA, Biere A. The effects of host weight at parasitism on fitness correlates of the gregarious koinobiont parasitoid Microplitis tristis and consequences for food consumption by its host, Hadena bicruris. Entomol. Exp. Appl. 2003;108:95–106. doi: 10.1046/j.1570-7458.2003.00072.x. DOI

Nicol CMY, Mackauer M. The scaling of body size and mass in a host‐parasitoid association: influence of host species and stage. Entomol. Exp. Appl. 1999;90:83–92. doi: 10.1046/j.1570-7458.1999.00425.x. DOI

Polis GA, Myers CA, Holt RD. The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu. Rev. Ecol. Syst. 1989;20:297–330. doi: 10.1146/annurev.es.20.110189.001501. DOI

Nakashima Y, Senoo N. Avoidance of ladybird trails by an aphid parasitoid Aphidius ervi: active period and effects of prior oviposition experience. Entomol. Exp. Appl. 2003;109:163–166. doi: 10.1046/j.1570-7458.2003.00094.x. DOI

Bezděk J, Baselga A. Revision of western Palaearctic species of the Oulema melanopus group, with description of two new species from. Europe (Coleoptera: Chrysomelidae: Criocerinae). Acta Ent. Mus. Nat. Pra. 2015;55:273–304.

Skuhrovec J, et al. Insecticidal activity of two formulations of essential oils against the cereal leaf beetle. Acta Agr. Scand. B-S. P. 2018;68:489–495.

Lucas É, Coderre D, Brodeur J. Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology. 1998;79:1084–1092. doi: 10.1890/0012-9658(1998)079[1084:IPAAPC]2.0.CO;2. DOI

Snyder WE, et al. Complementary biocontrol of aphids by the ladybird beetle Harmonia axyridis and the parasitoid Aphelinus asychis on greenhouse roses. Biol. Control. 2004;30:229–235. doi: 10.1016/j.biocontrol.2004.01.012. DOI

Nakashima Y, Birkett MA, Pye BJ, Powell W. Chemically mediated intraguild predator avoidance by aphid parasitoids: interspecific variability in sensitivity to semiochemical trails of ladybird predators. J. Chem. Ecol. 2006;32:1989–1998. doi: 10.1007/s10886-006-9123-y. PubMed DOI

Meindl P, Kromp B, Bartl B, Ioannidou E. Arthropod natural enemies of the cereal leaf beetle (Oulema melanopus L.) in organic winter wheat fields in Vienna, Eastern Austria. IOBC wprs Bulletin. 2001;24:79–86.

Evans EW. Lady beetles as predators of insects other than Hemiptera. Biol. Control. 2009;51:255–267. doi: 10.1016/j.biocontrol.2009.05.011. DOI

Nakashima Y, Birkett MA, Pye BJ, Pickett JA, Powell W. The role of semiochemicals in the avoidance of the seven-spot ladybird, Coccinella septempunctata, by the aphid parasitoid, Aphidius ervi. J. Chem. Ecol. 2004;30:1103–1116. doi: 10.1023/B:JOEC.0000030266.81665.19. PubMed DOI

Meisner M, Harmon JP, Harvey CT, Ives AR. Intraguild predation on the parasitoid Aphidius ervi by the generalist predator Harmonia axyridis: the threat and its avoidance. Entomol. Exp. Appl. 2011;138:193–201. doi: 10.1111/j.1570-7458.2010.01090.x. DOI

Snyder WE, Ives AR. Interactions between specialist and generalist natural enemies: parasitoids, predators, and pea aphid biocontrol. Ecology. 2003;84:91–107. doi: 10.1890/0012-9658(2003)084[0091:IBSAGN]2.0.CO;2. DOI

Brodeur J, Rosenheim JA. Intraguild interactions in aphid parasitoids. Entomol. Exp. Appl. 2000;97:93–108. doi: 10.1046/j.1570-7458.2000.00720.x. DOI

Boivin G, Martel V. Size-induced reproductive constraints in an egg parasitoid. J. Insect. Physiol. 2012;58:1694–1700. doi: 10.1016/j.jinsphys.2012.10.014. PubMed DOI

Harvey JA, Harvey IF, Thompson DJ. Lifetime reproductive success in the solitary endoparasitoid, Venturia canescens. J. Insect. Behav. 2001;14:573–593. doi: 10.1023/A:1012219116341. DOI

Segoli M, Rosenheim JA. The effect of body size on oviposition success of a minute parasitoid in nature. Ecol. Entomol. 2015;40:483–485. doi: 10.1111/een.12194. DOI

Segoli M, Rosenheim JA. Limits to the reproductive success of two insect parasitoid species in the field. Ecology. 2013;94:2498–2504. doi: 10.1890/13-0262.1. PubMed DOI

Song H, Meng L, Li B. Fitness consequences of body-size-dependent parasitism in a gregarious parasitoid attacking the 7-spot ladybird, Coccinella septempunctata (Coleoptera: Coccinellidae) Biol. Control. 2017;113:73–79. doi: 10.1016/j.biocontrol.2017.07.006. DOI

R. Core Team R. A language and environment for statistical computing. R Foundation for Statistical Computing (R Core Team, Vienna, 2017).

Genetic analysis reveals conspecificity of two nominal species of Anaphes fairyflies (Hymenoptera: Mymaridae), egg parasitoids of Oulema leaf beetle (Coleoptera: Chrysomelidae) pests of cereal crops in Europe and of rice in East Asia

An intergenerational approach to parasitoid fitness determined using clutch size

Effect of host switching simulation on the fitness of the gregarious parasitoid Anaphes flavipes from a novel two-generation approach