A dearth of data: fitting parasitoids into ecological networks

Abstract

Studying parasitoids can provide insights into global diversity estimates, climate change impacts, and agroecosystem service provision. However, this potential remains largely untapped due to a lack of data on how parasitoids interact with other organisms. Ecological networks are a useful tool for studying and exploiting the impacts of parasitoids, but their construction is hindered by the magnitude of undescribed parasitoid species, a sparse knowledge of host ranges, and an under-representation of parasitoids within DNA-barcode databases (we estimate <5% have a barcode). Here, we advocate the use of DNA metabarcoding to construct the host-parasitoid component of multilayer networks. While the incorporation of parasitoids into network-based analyses has far ranging applications, we focus on its potential for assessing ecosystem service provision within agroecosystems. Utility of host-parasitoid networks with a focus on agricultureHost-parasitoid dynamics have been a major focus of ecological and evolutionary study since the early 20th century due to the essential role parasitoids play within ecological communities, and their function as biocontrol agents (Box 1). The economic value of natural pest control is estimated to be $4.5 billion annually in the USA alone [1]. With recent bans on insect pesticides, as well as the prevalence of insecticide resistance, usage of biocontrol agents is likely to increase in the near future [2]. Release of parasitoids to control pests in closed systems, such as the widespread use of Encarsia formosa to control greenhouse whitefly (Trialeurodes vaporariorum) [3], is standard agricultural practice, and a range of parasitoid species are commercially available. Similarly, parasitoids have successfully been used in classical biological control (see Glossary). Anagyrus lopezi has been spectacularly successful against cassava mealybug in Africa, with savings estimated between US$8 billion and US$20 billion over 40 years [4]. Parasitoids are increasingly being discussed in the context of conservation biological control (CBC) [2,3,5]. However, the focus of host-parasitoid research mostly concerns direct interactions between agricultural pests and their parasitoids (Figure 1A). Relatively little is known about interactions between parasitoids and non-pest hosts (i.e., complete host ranges), other parasitoids, and predators (Figure 1B,C) [6] occurring within agricultural and natural systems. There is a growing realisation that these 'non-target' interactions can influence the utility of parasitoids as natural biological control agents via indirect effects, that is, interactions acting between two species that are mediated by one or more additional species (Figure 2) [7][8][9]. The impacts of these indirect interactions have been shown in experimental and field settings; for example, Sanders and van Veen (2012) found the absence of one parasitoid species can lead to the extinction of another via competitive exclusion between their two host species [9], and Cronin ( 2007) demonstrated that tw...

Aphelinus nigritus‐induced transgenerational fecundity compensation in parasitized Melanaphis sorghi

“…Our findings provide insight into the complexity of a parasitoid‐aphid interaction. In agroecosystems, parasitoids are generally viewed as ecosystem service providers because they exert top‐down control on pests (Miller et al, 2021). However, this viewpoint does not consider aphid pests' responses, or how these responses may shape parasitoid‐aphid dynamics.…”

A curated DNA barcode reference library for parasitoids of northern European cyclically outbreaking geometrid moths

“…At the individual level, field‐collected parasitoid eggs, larvae, pupae, and adults can be readily identified based on barcode sequences, and rates of parasitism by externally inconspicuous endoparasitoids can be estimated using metabarcoding of DNA extracted from single host larvae (cf. Kitson et al, 2019 ; Miller, Polaszek, & Evans, 2021 ). For the latter type of studies, the availability of a parasitoid barcode reference library facilitates in silico validation of mini‐barcode amplification primers, as well as design of blocking oligomers suppressing simultaneous amplification of host DNA (Nakadai & Kawakita, 2017 ).…”

“…Techniques based on DNA barcoding and genome‐level markers can effectively resolve complexes of cryptic or near‐cryptic species, but of the natural enemies of the focal moths, only the microgastrine genera Protapanteles and Cotesia have hitherto been investigated using molecular tools (Ruohomäki et al, 2013 ). Barcoding and metabarcoding approaches also allow obtaining data directly from herbivore larvae, without a need to rear hosts and parasitoids to adults (Kitson et al, 2019 ; Miller, Aguilera, et al, 2021 ; Miller, Polaszek, & Evans, 2021 ; Nakadai & Kawakita, 2017 ; Sow et al, 2019 ; Volf et al, 2017 ). Furthermore, when a reference barcode library for relevant parasitoids is available, their local community structures and abundances can be estimated based on large‐scale material obtained through, for example, Malaise trapping (Barsoum et al, 2019 ; DeWaard et al, 2019 ; Lue et al, 2021 ; Roslin et al, 2022 ).…”

Overcoming the pitfalls of merging dietary metabarcoding into ecological networks

“…trophic and non‐trophic interactions; Pilosof et al., 2017) at different levels of biological organisation (i.e. bipartite plant–herbivore and herbivore–parasitoid networks integrated together to form tripartite plant–herbivore–parasitoid networks; Miller et al., 2021) to provide both conceptual and applied advances (e.g. identifying the optimal plant communities in field margins that provide multiple ecosystem services; Windsor et al., 2021).…”