Extending the “Ecology of Fear” Beyond Prey: Reciprocal Nonconsumptive Effects Among Competing Aphid Predators

Abstract

Nonconsumptive effects of predators on prey are well known, but similar effects among competing predators are not. Aphidophagous insect larvae are notorious for cannibalism and intraguild predation, as they compete for aggregated but ephemeral prey. We tested for indirect effects of competitors on the development of Coleomegilla maculata DeGeer and Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae), and a green lacewing, Chrysoperla carnea Stephens (Neuroptera: Chrysopidae), with all larvae reared on eggs of Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Control larvae were reared singly, while treatment larvae were reared pairwise, with either a conspecific or heterospecific, in partitioned Petri dishes that allowed the passage of chemical cues. Larvae of C. maculata, a dietary generalist, appeared stressed by the presence of competing larvae, whether con- or heterospecific, and suffered fitness costs (longer pupation times, lower male adult mass). In contrast, H. convergens and C. carnea, both aphid specialists, responded to competing larvae with accelerated development, and without any apparent costs in terms of adult size or reproductive performance. Adult C. carnea in some treatments were heavier than solitary controls, suggesting a higher consumption rate by the induced phenotype, and those exposed to H. convergens began oviposition earlier. Thus, the phenotypes induced in the specialized aphid predators were adaptive for development in aphid colonies, whereas that induced in the generalist was not. These results indicate that nonconsumptive effects are not simply a vertical force acting on prey, but can also impact conspecific and heterospecific competitors on the same trophic level.

Beyond killing: intra‐ and interspecific nonconsumptive effects among aphidophagous competitors

“…The developmental response of ESL to the presence of conspecific or heterospecific competitor cues supports our second hypothesis and appears consistent with the 'behavioral hypothesis' of survivor life history (Ball & Baker, 1996;Noonburg & Nisbet, 2005), but appears inconsistent with the 'physiological hypothesis' of survivor life history. Generalist predators often develop on a wider range of prey, few of which would present the hazardous environment of an aphid colony (Michaud et al, 2016), and thus we infer that ESL has no history of directional selection for adaptive developmental plasticity in response to the highly competitive environment of an aphid colony. The threat of competitors exerted various fitness costs on developing ESL larvae (slower development and lower reproductive performances) and these life-history changes cannot be construed as adaptive tactics for avoiding the predation stress (Ball & Baker, 1996).…”

“…The first design followed Michaud et al (2016) and used two Petri-dishes to study the interactions between pairs of larvae. The first design followed Michaud et al (2016) and used two Petri-dishes to study the interactions between pairs of larvae.…”

“…Experiments used two forms of partitioned plastic Petri-dishes (9.0 cm diameter × 2.0 cm height). The first design followed Michaud et al (2016) and used two Petri-dishes to study the interactions between pairs of larvae. Each dish had a cyclic hole (3.0 cm diameter) either in the top or the bottom of the dish.…”

“…These two mechanisms are often treated as dichotomous alternatives (Creel & Christianson, 2008). The ecology of fear -the nonconsumptive effects (NCEs) of predators on their prey -has received increased attention over the past decade, not only for its implications on prey behaviour and development, but also for its higher order impacts for ecosystem dynamics (Ohgushi et al, 2012;Michaud et al, 2016). These impacts can be equivalent to or higher than Intra-and interspecific nonconsumptive effects 795 that of direct predation, and can sometimes change community composition more than direct interactions (Preisser et al, 2005).…”

“…A partitioned Petri-dish was used to examine the NCEs between conspecific or heterospecific larval pairs (Michaud et al, 2016). The configuration of this dish was modified to permit investigation of the NCEs between multiple heterospecific larvae, preventing them from physical contact, while allowing contact with volatile cues from each other.…”