Facultative production of multiple-egg clutches in a quasi-gregarious parasitoid: fitness gains for offspring at low developmental temperature

  • Peng-Cheng Liu
  • Ju Luo
  • Shuo Tian
  • Shao-Ying Wen
  • Jian-Rong Wei
  • De-Jun Hao
Original Article


In the quasi-gregarious parasitoid wasp Anastatus disparis, a mother may lay more than one egg in a host during a single host encounter. This is conventionally known as self-superparasitism and, since only one adult offspring can complete development on the host, it may represent a waste of eggs and time. However, this behavior may be better described as “multiple-egg clutches,” which differs fundamentally from self-superparasitism and has seldom been addressed. The potential benefits of laying multiple-egg clutches are currently unclear, and we therefore aimed to investigate them in A. disparis. First, our results showed that production of multiple-egg clutches by A. disparis is not due to a lack of discrimination between unparasitized and parasitized hosts, as females preferred to lay eggs in unparasitized hosts. It was also unrelated to the age of the female or her mating status, or to the presence of conspecific females. However, compared to the temperatures of 26 and 32 °C, we observed that the frequency of multiple-egg clutches increased at the temperature of 20 °C. In addition, low developmental temperatures significantly decreased the rate of successful wasp eclosion from hosts in which a single egg was deposited, and this rate was increased by laying multiple-egg clutches. These results suggest that female A. disparis adults produce multiple-egg clutches to increase the probability of obtaining offspring from the host, and may have the ability to regulate oviposition and reproduction strategy based on environmental temperature.

Significance statement

Anastatus disparis exhibited an oviposition behavior of facultative production of multiple-egg clutches, which is not due to a lack of host discrimination, or due to the age of the female or her mating status nor the presence of conspecific females. However, our results suggest that A. disparis adults produce multiple-egg clutches when it increased the probability of obtaining offspring from the host, and may have the ability to regulate their oviposition strategy based on environmental temperature.


Conspecific superparasitism Host discrimination Multiple-egg clutches Quasi-gregarious Self-superparasitism 



This work was supported by the Doctorate Fellowship Foundation of Nanjing Forestry University and National Science Foundation of China (30500392 and 31470650).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Alalouni U, Schädler M, Brandl R (2013) Natural enemies and environmental factors affecting the population dynamics of the gypsy moth. J Appl Entomol 137:721–738CrossRefGoogle Scholar
  2. Avci M (2009) Parasitoid complex and new host plants of the gypsy moth, Lymantria dispar L. in the lakes district, Turkey. J Anim Vet Adv 8:1402–1405Google Scholar
  3. Bell HA, Marris GC, Prickett AJ, Edwards JP (2005) Influence of host size on the clutch size and developmental success of the gregarious ectoparasitoid Eulophus pennicornis (Nees) (Hymenoptera: Eulophidae) attacking larvae of the tomato moth Lacanobia oleracea (L.) (Lepidoptera: Noctuidae). J Exp Biol 208(16):3199–3209CrossRefPubMedGoogle Scholar
  4. Blumberg D, Luck RF (1990) Differences in the rates of superparasitism between two strains of Comperiella bifasciata (Howard) (Hymenoptera: Encyrtidae) parasitizing California red scale (Homoptera: Diaspididae): an adaptation to circumvent encapsulation? Ann Entomol Soc Am 83(3):591–597CrossRefGoogle Scholar
  5. Boulton RA, Collins LA, Shuker DM (2015) Beyond sex allocation: the role of mating systems in sexual selection in parasitoid wasps. Biol Rev 90:599–627CrossRefPubMedGoogle Scholar
  6. Brown MW (1984) Literature review of Ooencyrtus kuvanae [Hym.: Encyrtidae], an egg parasite of Lymantria dispar [Lep, Lymantriidae]. Entomophaga 29:249–265CrossRefGoogle Scholar
  7. Brown MW, Cameron EA (1982) Natural enemies of Lymantria-dispar lep, lymantriidae eggs in central Pennsylvania, USA, and a review of the world literature on natural enemies of Lymantria-dispar eggs. Entomophaga 27:311–322CrossRefGoogle Scholar
  8. Couchoux C, Seppä P, van Nouhuys S (2015) Behavioural and genetic approaches to evaluate the effectiveness of deterrent marking by a parasitoid wasp. Behaviour 152(9):1257–1276CrossRefGoogle Scholar
  9. Crossman SS (1925) Two imported egg parasites of the gipsy moth, Anastatus bifasciatus Fonsc and Schedius kuvanae Howard. J Agric Res 30:643–675Google Scholar
  10. Godfray HCJ (1987) The evolution of clutch size in parasitic wasps. Am Nat 129:221–233CrossRefGoogle Scholar
  11. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, PrincetonGoogle Scholar
  12. Hardy ICW, Griffiths NT, Godfray HCJ (1992) Clutch size in a parasitoid wasp: a manipulation experiment. J Anim Ecol 61(1):121–129CrossRefGoogle Scholar
  13. Hoy MA (1976) Establishment of gypsy moth parasitoids in North America: an evaluation of possible reasons for establishment or non-establishment. In: Anderson JF, Kaya HK (eds) Perspectives in forest entomology. Academic Press, New York, pp 215–232Google Scholar
  14. Hubbard SF, Marris G, Reynolds A, Rowe GW (1987) Adaptive patterns in the avoidance of superparasitism by solitary parasitic wasps. J Anim Ecol 56:387–401CrossRefGoogle Scholar
  15. Kapranasa A, Luck RF (2012) Dynamic virulence in a parasitoid wasp: the influence of clutch size and sequential oviposition on egg encapsulation. Anim Behav 83(3):833–838CrossRefGoogle Scholar
  16. King BH, Skinner SW (1991) Proximal mechanisms of the sex ratio and clutch size responses of the parasitoids wasps Nasonia vitripennis to parasitized hosts. Anim Behav 42:23–32CrossRefGoogle Scholar
  17. Kurir A (1944) Anastatus disparis Ruschka Eiparasit des Lymantria dispar L. J Appl Entomol 30:551–586Google Scholar
  18. Li BJ, Lou JX (1992) Preliminary studies on Anastatus disparis (Hymenoptera: Eupelmidae), an egg parasitoid of gypsy moth. Chinese J Biol Control 144Google Scholar
  19. Li ZY, Yao DF, Chen YM, Feng JH, Yan GZ, Shi J (2001) Parasitioids and alternate hosts of gypsy moth in Beijing area. J B Forestry Univ 23(5):39–42Google Scholar
  20. Liu S, Zhao B, Bonjour E (2012) Host marking and host discrimination in phytophagous insects. In: Liu T, Kang L (eds) Recent advances in entomological research. Springer, Dordrecht, pp 73–85Google Scholar
  21. Liu PC, Wei JR, Wang JJ, Liu JX, Dong LJ (2015) Relationship between the environmental temperatures and development of Anastatus disparis (Ruschka) (Hymenoptera: Eupelmidae) and the sex ratio control of the offspring. Forest Pest Dis 34:9–14Google Scholar
  22. Liu PC, Men J, Zhao B, Wei JR (2017) Fitness-related offspring sex allocation of Anastatus disparis, a gypsy moth egg parasitoid, on different-sized host species. Entomol Exp Appl 163:281–286CrossRefGoogle Scholar
  23. Mackauer M (1990) Host discrimination and larval competition in solitary endoparasitoids. In: Mackauer M, Ehler LE, Roland J (eds) Critical issues in biological control. Intercept Ltd, Andover, pp 41–62Google Scholar
  24. Mayhew PJ, Hardy ICW (1998) Nonsiblicidal behavior and the evolution of clutch size in bethylid wasps. Am Nat 151:409–424CrossRefPubMedGoogle Scholar
  25. Michaud JP, Mackauer M (1995) The oviposition behavior of Monoctonus paulensis (Ashmead) (Hymenoptera: Aphidiidae): factors influencing reproductive allocation to hosts and host patches. Ann Entomol Soc Am 88:220–226CrossRefGoogle Scholar
  26. Parker GA, Courtney SP (1984) Models of clutch size in insect oviposition. Theor Popul Biol 26:27–48CrossRefGoogle Scholar
  27. Pennacchio F, Strand MR (2006) Evolution of developmental strategies in parasitic Hymenoptera. Ann Rev Entomol 51(1):233–258Google Scholar
  28. Roitberg BD, Sircom J, Roitberg CA, van Alphen JJ, Mangel M (1993) Life expectancy and reproduction. Nature 364(6433):108CrossRefPubMedGoogle Scholar
  29. Rosenheim JA, Hongkham D (1996) Clutch size in an obligately siblicidal parasitoid wasp. Anim Behav 51:841–852CrossRefGoogle Scholar
  30. Rosenheim JA, Rosen D (1991) Foraging and oviposition decisions in the parasitoid Aphytis lingnanensis: distinguishing the influences of egg load and experience. J Anim Ecol 60(3):873–893CrossRefGoogle Scholar
  31. Santolamazza CS, Cordero RA (2003) Egg load and adaptive superparasitism in Anaphes nitens, an egg parasitoid of the Eucalyptus snout-beetle Gonipterus scutellatus. Entomol Exp Appl 106:127–134CrossRefGoogle Scholar
  32. Spanoudis CG, Andreadis SS (2012) Temperature-dependent survival, development, and adult longevity of the koinobiont endoparasitoid Venturia canescens, (Hymenoptera: Ichneumonidae) parasitizing Plodia interpunctella, (Lepidoptera: Pyralidae). J Pest Sci 85(1):75–80CrossRefGoogle Scholar
  33. Strand MR (1986) The physiological interactions of parasitoids with their hosts and their influence on reproductive strategies. In: Waage J, Greathead D (eds) Insect parasitoids. Academic Press, London, pp 97–136Google Scholar
  34. Takasu K, Hirose Y (1988) Host discrimination in the parasitoid Ooencyrtus nezarae: the role of the egg stalk as an external marker. Entomol Exp Appl 47:45–48CrossRefGoogle Scholar
  35. Ueno T (1994) Self-recognition by the parasitic wasp Itoplectis naranyae (Hymenoptera: Ichneumonidae). Oikos 70:333–339CrossRefGoogle Scholar
  36. van Alphen JJM, Visser ME (1990) Superparasitism as an adaptive strategy for insect parasitoids. Annu Rev Entomol 35:59–79CrossRefPubMedGoogle Scholar
  37. van Dijken MJ, Waage JK (1987) Self- and conspecific superparasitism by the egg parasitoid Trichogramma evanescens. Entomol Exp Appl 43:183–192CrossRefGoogle Scholar
  38. Visser ME (1993) Adaptive self- and conspecific superparasitism in the solitary parasitoid Leptopilina heterotoma (Hymenoptera: Eucoilidae). Behav Ecol 4:22–28CrossRefGoogle Scholar
  39. Visser ME, van Alphen JJM, Nell HW (1990) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of the number of parasitoids depleting a patch. Behaviour 114:21–36CrossRefGoogle Scholar
  40. Visser ME, van Alphen JJM, Nell HW (1992) Adaptive superparasitism and patch time allocation in solitary parasitoids: the influence of pre-patch experience. Behav Ecol Sociobiol 31:163–171CrossRefGoogle Scholar
  41. Völkl W, Mackauer M (1990) Age-specific pattern of host discrimination by the aphid parasitoid Ephedrus californicus Baker (Hymenoptera: Aphidiidae). Can Entomol 122:349–361CrossRefGoogle Scholar
  42. Waage JK (1986) Family planning in parasitoids: adaptive patterns of progeny and sex allocation. In: Waage JK, Greathead DJ (eds) Insect parasitoids. Academic Press, London, pp 63–95Google Scholar
  43. Wang JJ, Liu XB, Zhang YA, Wen C, Wei JR (2014) The reproductive capability of Ooencyrtus kuvanae, reared on eggs of the factitious host Antheraea pernyi. J Appl Entomol 138:267–272CrossRefGoogle Scholar
  44. Yamada YY, Sugaura K (2003) Evidence for adaptive self-superparasitism in the dryinid parasitoid Haplogonatopus atratus, when conspecifics are present. Oikos 103:175–181CrossRefGoogle Scholar
  45. Yan JJ, Xu CH, Gao WC, Li GW, Yao DF, Zhang PY et al (1989) Parasites and predators of forest pest. China Forestry Publishing House, BeijingGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Peng-Cheng Liu
    • 1
    • 2
  • Ju Luo
    • 1
    • 2
  • Shuo Tian
    • 1
    • 2
  • Shao-Ying Wen
    • 1
    • 2
  • Jian-Rong Wei
    • 3
  • De-Jun Hao
    • 1
    • 2
  1. 1.Co-Innovation Center for the Sustainable Forestry in Southern ChinaNanjing Forestry UniversityNanjingChina
  2. 2.College of ForestryNanjing Forestry UniversityNanjingChina
  3. 3.College of Life ScienceHebei UniversityBaodingChina

Personalised recommendations