The effect of obligate hyperparasitoids on biological control: Differential vulnerability of primary parasitoids to hyperparasitism can mitigate trophic cascades

Abstract

Highlights-Cotesia vestalis was a dominant primary parasitoid of Plutella xylostella.-It was also a secondary host to three obligate hyperparasitoid species.-At low hyperparasitism, C. vestalis limited hosts available to competitors. -As C. vestalis population declined, competitors parasitized more of available hosts.-Species that are invulnerable to hyperparasitism took over role of the vulnerable. Graphical abstractAbstract : Obligate hyperparasitoids are widely considered an important ecological disturbance to biological control of insect pests, as they develop at the expense of primary parasitoids. However, supporting evidence is largely derived from direct trophic interactions in simple food webs. Yet, a multitude of insect pest populations simultaneously support development of several primary parasitoid species in horticultural and natural systems. Since primary parasitoid species in a community can differ in vulnerability to obligate hyperparasitoids, it is desirable to establish if the invulnerable primary parasitoids can take advantage of reduced competition from affected species by increasing their contribution to total primary parasitism levels thereby mitigating effects of hyperparasitism on biological control. To investigate this question, populations of the diamondback moth, Plutella xylostella (Linnaeus) (Plutellidae), its primary parasitoids and hyperparasitoids were monitored on unsprayed cabbage plots at weekly intervals over six consecutive years. Cotesia vestalis (Haliday) (Braconidae), a dominant primary parasitoid in this system, was a secondary host to three obligate hyperparasitoids: Mesochorus sp. (Ichneumonidae), Eurytoma sp. (Eurytomidae) and Pteromalus sp. (Pteromalidae). The higher efficiency of C. vestalis in utilizing younger host larvae at lower hyperparasitism levels limited host availability to other major primary parasitoids. But, as hyperparasitism levels increased and its populations declined, populations of Oomyzus sokolowskii (Kurdjumov) (Eulophidae) and Diadromus collaris (Gravenhorst) (Ichneumonidae) increased significantly as they parasitized a greater proportion of available hosts. As a consequence, the impact of hyperparasitoids did not result in trophic cascades, as their impact on total primary parasitism levels and infestation levels was insignificant. This study shows that primary parasitoid species that are invulnerable to hyper-parasitism can take over the function of vulnerable ones in communities where interspecific interactions among species are strong. Thus, an approach that considers both direct and indirect effects of hyperparasitoids in primary parasitoid communities improves our understanding of the net impact of hyperparasitism on biological control of insect pests.

Reproductive and Developmental Biology of Acroclisoides sinicus, a Hyperparasitoid of Scelionid Parasitoids

“…A related question concerns the ecological impact of such hyperparasitoid on the global natural control provided by native egg parasitoid guilds and their role in the ecosystem. The recent discoveries of adventive A. sincus in newly invaded areas of Europe and North America suggest that it is likely to become a permanent part of the local fauna, but the impact of this species to the ecosystem of the North American and European fauna is a matter to be assessed in the future [ 38 ]. Biological traits presented in our work can explain many aspects of biological and ethological features under field conditions and can be helpful for future planning of research with such complicated parasitoid species, where highly specific optimal timing of host suitability within the entire trophic chain is fundamental for the success of the parasitoid’s reproduction.…”

Biotic Interactions as Mediators of Biological Invasions: Insights from South Africa

“…Hyperparasitoids were also found to feed on the cocoons of primary parasitoid larvae and were influenced by the abundance and timing of the latter (Mosiane et al 2003;Nofemela and Kfir 2005). Therefore, the complexity of these tri-trophic relationships, including potential density-dependent and cascading top-down effects, are likely to modulate the dynamics of these pests and invasive populations (Nofemela 2013).…”

Cascading effects of herbivore protective symbionts on hyperparasitoids

“…In addition, if a protective symbiont causes a local reduction in an otherwise abundant primary parasitoid, it may allow increased food web diversity by providing opportunities for other primary parasitoids. High numbers of specialist hyperparasitoids have been shown to suppress dominant primary parasitoids in the field (Nofemela, 2013), allowing other primary parasitoid species to flourish. Likewise, different primary parasitoids have different levels of vulnerability to protection provided by different strains of H. defensa (Asplen et al, 2014;Cayetano & Vorburger, 2015;McLean & Godfray, 2015), and this asymmetry means that some primary parasitoids actually gain a relative advantage in the presence of the symbiont, as it releases them from competition (Rothacher et al, 2016).…”