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

Abstract

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 hyperparasitism 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.