Protection via parasitism: Datura odors attract parasitoid flies, which inhibit Manduca larvae from feeding and growing but may not help plants

Abstract

Insect carnivores frequently use olfactory cues from plants to find prey or hosts. For plants, the benefits of attracting parasitoids have been controversial, partly because parasitoids often do not kill their host insect immediately. Furthermore, most research has focused on the effects of solitary parasitoids on growth and feeding of hosts, even though many parasitoids are gregarious (multiple siblings inhabit the same host). Here, we examine how a gregarious parasitoid, the tachinid fly Drino rhoeo, uses olfactory cues from the host plant Datura wrightii to find the sphingid herbivore Manduca sexta, and how parasitism affects growth and feeding of host larvae. In behavioral trials using a Y-olfactometer, female flies were attracted to olfactory cues emitted by attacked plants and by cues emitted from the frass produced by larval Manduca sexta. M. sexta caterpillars that were parasitized by D. rhoeo grew to lower maximum weights, grew more slowly, and ate less of their host plant. We also present an analytical model to predict how tri-trophic interactions change with varying herbivory levels, parasitization rates and plant sizes. This model predicted that smaller plants gain a relatively greater benefit compared to large plants in attracting D. rhoeo. By assessing the behavior, the effects of host performance, and the variation in ecological parameters of the system, we can better understand the complex interactions between herbivorous insects, the plants they live on and the third trophic level members that attack them.

Costs and benefits of omnivore-mediated plant protection: effects of plant-feeding on Salix growth more detrimental than expected

“…Given the lack of knowledge, determining how often or under what circumstances natural enemies fail to provide benefits to plants, despite reducing herbivore damage, is not straightforward. Nonetheless, we do know that even the most voracious of predators do not always decrease herbivore damage to plants and their value as ‘bodyguards’ can vary with ecological conditions (Dicke 2009; Kaplan 2012; Wilson and Woods 2015) and quality of plant genotypes exposed to (Stephan et al 2016). In the case of O. marginalis , its plant protective role has been assumed from highly efficient egg predation; as most of the plant damage is caused by late-instar beetle larvae, predation on eggs and early-instar larvae represents the most important contribution to pest control (Björkman et al 2003).…”

Innate and Learned Olfactory Responses in a Wild Population of the Egg ParasitoidTrichogramma(Hymenoptera: Trichogrammatidae)

“…All herbivores were removed by hand from 10 D. wrightii plants (any M. sexta or M. quinquemaculata larvae and eggs, as well as other common herbivorous insects) and two fifth-instar M. sexta larvae were placed on plant and allowing them to feed for 48 h, inducing VOC production in D. wrightii (Wilson and Woods 2015) . Datura wrightii plants were from four different patches at our field site, spanning 8 km.…”

“…Nevertheless, they have come under recent criticism as not always being ecologically applicable (Ballhorn and Kautz 2013). In some instances, incorporating ecological variation into Y-olfactometer experiments can generate alternative conclusions (Wilson and Woods 2015). Here, we use a combination approach that employs Y-olfactometers in the laboratory and in the field, where we attempt to capture ecological variance (differences among plants, levels of herbivory, induction, and abiotic variation) that might modify insect behavior in important ways.…”

Within-host competition drives energy allocation trade-offs in an insect parasitoid

“…Furthermore, biologists have long examined patterns of body size over large spatial scales (Blackburn, Gaston & Loder, 1999;Mousseau, 1997), and examined how body size can affect complex community food webs (Jonsson, Cohen & Carpenter, 2005). Examining the relative size of different body parts (allometric scaling relationships (Gould, 1966)) has become an important analytical tool alongside measurements of body size in diverse research topics including sexual selection (Emlen & Nijhout, 2000;McCullough & Emlen, 2013), Drino rhoeo attacks caterpillars of the hawkmoth Manduca sexta and Manduca quinquemaculata (Bernays & Woods, 2000;Mira & Bernays, 2002;Wilson & Woods, 2015) frequently at our field site in southeastern Arizona (near Portal and the Chiricahua mountains). Female flies target fourth-and fifth-instar caterpillars, laying eggs on the surface of the caterpillar after which fly larvae shortly (within 20 min) emerge and burrow into the caterpillar hemocoel where they grow and develop.…”

“…Developing tachinid larvae typically completely consume the bodies of their hosts, resulting in host-death. Previous work has demonstrated that D. rhoeo can have a strong impact on the growth and development of hosts post-parasitization, affecting growth, weight and feeding habits (Wilson & Woods, 2015) which may, in turn, affect the amount of resources available to the parasitoids.…”