Generalist Predators Disrupt Biological Control by a Specialist Parasitoid

Abstract

Two broad classes of arthropod natural enemies attack insect herbivores: specialists and generalists. The tight dynamical linkage of specialist natural enemies and their prey may make the specialists able to respond numerically to, and perhaps suppress, herbivore outbreaks. Because generalist predators may attack not only herbivores, but also the herbivores' specialist natural enemies, generalist predators may disrupt control of herbivore populations rather than contribute to it. We examined interactions between pea aphids (Acyrthosiphon pisum), a specialist parasitoid wasp (Aphidius ervi) that attacks the aphids, and a common generalist predator, carabid beetles (primarily Pterostichus melanarius). In two field experiments in alfalfa, we manipulated carabid densities to measure their direct (through predation) and indirect (through intraguild predation on A. ervi) impact on aphid population dynamics. The first experiment was initiated when plants were short (following cutting), and carabid predation of aphids led to an immediate reduction in aphid densities. This reduction was short‐lived, however, because carabids reduced parasitism, leading to higher aphid population growth rates. Therefore, although the immediate direct effect of carabids was a reduction in aphid densities, this was offset in the longer term by the indirect effect of carabids disrupting the control of aphids by parasitoids. The second experiment was initiated after plants had regrown following cutting. When plants were tall, carabids had no direct impact on aphid densities. Nonetheless, the slow indirect effect of carabids on aphid densities through reduction in parasitism still occurred, leading to higher aphid population growth rates in the presence of carabids. Additional laboratory experiments demonstrated that carabids are able to climb into plants and prey upon the immobile parasitoid pupae (“mummies”), whereas antipredator behaviors of the aphids protect them from predation by carabids when plants are tall. Overall, carabid predation caused an immediate but ephemeral decrease in aphid density. In contrast, the indirect positive effect on aphid density caused by reducing parasitism developed later but persisted longer. Thus the generalist carabid primarily acted as an intraguild predator, interrupting aphid population control by the specialist parasitoid.

Seasonal variation in top-down and bottom-up processes in a grassland arthropod community

“…We hypothesize that this indirect effect is caused by cursorial spiders preying on other predators. Our removal of cursorial spiders (extreme generalist predators) reduced intraguild predation within the system (Rosenheim et al 1993;Snyder and Ives 2001) allowing other generalist predators to maintain control of herbivores, especially grazing herbivores. Since there was no net change in carnivore abundance, this explanation would be valid only if other predators were more efficient at consuming herbivores.…”

Intraguild interference and biocontrol effects of generalist predators in a winter wheat field

“…Therefore, predatory encounters between the latter and parasitoid hymenopterans also represent intraguild interference, and hymenopteran parasitoids or their parasitised hosts, respectively, can be preyed upon by carabid beetles and spiders (e.g. Heimpel et al 1997;Brodeur and Rosenheim 2000;Snyder and Ives 2001). Potentially, natural enemies can interfere negatively with the impact of aphid parasitoids (e.g.…”

“…Intraguild interference is a feature typical for polyphagous predator communities, and also a widespread phenomenon among generalist invertebrate predators occurring in arable land (e.g. Schaefer 1974;Rosenheim et al 1995;Guillebeau and All 1989;Kester and Jackson 1996;Dinter 1998;Sunderland et al 1997;Snyder and Ives 2001). In consequence, intraguild interference can be antagonistic to pest control and may even lead to an enhancement of the concerned prey population, if the main predator of this prey is substantially reduced by another predator (e.g.…”

Brood-size and sex-ratio variation in field populations of three species of solitary aphid parasitoids (Hymenoptera: Braconidae, Aphidiinae)

“…Also, there is apparently no absolute lower limit to host size in that eggs deposited in aphid embryos develop successfully although the eclosing wasps are much smaller than counterparts developing in larger aphids (Mackauer and Kambhampati 1988). Hyperparasitism (Sullivan and Völkl 1999) and predation (Colfer and Rosenheim 2001;Snyder and Ives 2001) could also cause sexspecific offspring mortality. For example, Dendrocerus carpenteri (Curtis) (Hymenoptera: Megaspilidae), a generalist hyperparasitoid of aphidiine prepupae and pupae inside mummified aphids, chooses hosts according to mummy size (Mackauer and Lardner 1995;Otto and Mackauer 1998).…”