A temporal trophic shift from primary parasitism to facultative hyperparasitism during interspecific competition between two coevolved scelionid egg parasitoids

Abstract

Understanding competition between scelionid parasitoids that exploit the same host may provide insight into strategies that allow coexistence on a shared resource.Competition studies typically focus on interactions between native and exotic parasitoids that do not share an evolutionary history; however, coevolved parasitoids may be more likely to demonstrate strategies to avoid or exploit a shared resource. We examined intrinsic and extrinsic competition between Asian Trissolcus japonicus (Ashmead) and T. cultratus (Mayr) (Hymenoptera: Scelionidae) associated with Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) that share an evolutionary history. Interspecific interactions were assessed by providing parasitized egg masses to each species at various intervals post-parasitism, and measuring host acceptance, developmental suitability, and guarding behaviour. Trissolcus japonicus showed high acceptance of parasitized hosts up to 72 h following oviposition by T. cultratus, despite a very poor developmental outcome. In contrast, T. cultratus generally avoided ovipositing in H. halys eggs containing T. japonicus early-instar larvae but did not avoid parasitizing H. halys that contained eggs and third instar larvae. The adaptive value of this behaviour was supported by developmental outcome: T. cultratus outcompeted T. japonicus eggs but not early-instar larvae, and a trophic shift occurred wherein T. cultratus developed as a facultative hyperparasitoid on third instar T. japonicus larvae. Trissolcus japonicus guarded egg masses 8-12× longer and displayed more aggressive interactions than T. cultratus, suggesting T. japonicus is the superior extrinsic competitor. Development as a facultative hyperparasitoid provided a competitive niche for Asian T. cultratus and confirms its instrinsic competitive superiority. This also occurs in a biologically distinct European population of T. cultratus, suggesting that facultative hyperparasitism as a competitive strategy is retained in geographically separated populations that have not coevolved with H. halys or T. japonicus.

Interspecific Competition between Trissolcus Japonicus and Trissolcus Mitsukurii, Two Promising Candidates for Biocontrol of Halyomorpha Halys

“…Previous studies on interspecific competition between T. japonicus and native European and Asian egg parasitoids [Anastatus bifasciatus (Geoffroy), Anastatus japonicus Ashmead (Hymenoptera, Eupelmidae), and Trissolcus cultratus (Mayr) (Hymenoptera, Scelionidae)] found strong aggressive behavior by T. japonicus females, but also by T. mitsukurii against the latter, as recently reported by Costi et al, 2022. However, successful competition is also affected by the time of arrival to the host eggs (Konopka et al, 2017a;Haye et al, 2021;Mi et al, 2021). Similarly, studies on interspecific competition involving T. mitsukurii within the parasitoid guild of Nezara viridula L. (Hemiptera, Pentatomidae) [Trissolcus basalis (Wollaston) and Telenomus nakagawai Watanabe (Hymenoptera, Scelionidae)] documented its aggressive behavior in host patch defense Field and Calbert, 1999;Nishimoto et al, 2015).…”

“…The sympatry of T. japonicus and T. mitsukurii as reported by recent field data both in Italy (Zapponi et al, 2021) and Europe in general (see Bout et al, 2021;Dieckhoff et al, 2021;Rot et al, 2021), and the potential opportunity to use these species in biological control programs against H. halys, stimulated a number of studies on their interactions with each other or with different species of the parasitoid guild, in order to assess possible pest control outcomes, as firstly evidenced by Konopka et al (2017aKonopka et al ( , 2017b, Haye et al (2021), Mi et al (2021) and successively by Costi et al (2022). Indeed, interspecific competition can potentially disrupt biological control programs, or cause synergism, or it may have no influence at all (Boivin and Brodeur, 2006;Casula et al, 2006;Mills, 2006;Ode et al, 2022).…”

Partial refuges from biological control due to intraspecific variation in protective host traits: a case study with the egg parasitoidTrissolcus japonicus

“…First, we calculated oviposition rate – the number of ovipositions divided by the time between the first and last oviposition, as an index of how efficiently T. japonicus exploited host egg masses. Second, because many egg parasitoids in the family Scelionidae, including T. japonicus , are known to engage in post-oviposition brood guarding that could affect how long they stay on egg masses of different sizes (Field 1998; Haye et al 2021), we also recorded the probability of extended brood guarding, defined as whether or not parasitoids remained on the host egg mass for at least 2 hours after the last oviposition, or until the end of the photophase of the first day (as on some larger egg masses, the last oviposition was within 2 hours of the end of the day; similar results were obtained with other criteria for defining extended guarding behaviour). Third, we determined how likely ovipositor rejections versus ovipositions were as parasitoids exploited patches of different hosts and egg mass sizes by scoring the probability of rejections rather than ovipositions (0, 1) over the temporal sequence of patch exploitation for each individual.…”

Performance of two egg parasitoids of brown marmorated stink bug before and after cold storage

“…However, a Swiss population of T. cultratus was found to be unable to attack fresh egg masses of H. halys. The Swiss population of this parasitoid is believed to be a different geographical strain of T. cultratus from that found attacking H. halys in China and other parts of the bug's native range and, therefore, not co-evolved with H. halys (Haye et al, 2021). Anyhow, T. cultratus is still under consideration as a parasitoid that could contribute to the control H. halys in the long-term (Haye et al, 2015).…”