Eating chemically defended prey: alkaloid metabolism in an invasive ladybird predator of other ladybirds (Coleoptera: Coccinellidae)

Abstract

SUMMARYBy comparison with studies of herbivore physiological adaptation to plant allelochemicals, work on predator physiological adaptation to potentially toxic prey has been very limited. Such studies are important in understanding how evolution could shape predator diets. An interesting question is the specificity of predator adaptation to prey allelochemicals, given that many predators consume diverse prey with different chemical defences. The ladybird Harmonia axyridis, an invasive species in America, Europe and Africa, is considered a significant predatory threat to native invertebrates, particularly other aphid-eating ladybirds of which it is a strong intraguild predator. Although ladybirds possess species-specific alkaloid defences, H. axyridis exhibits high tolerance for allospecific ladybird prey alkaloids. Nonetheless, it performs poorly on species with novel alkaloids not commonly occurring within its natural range. We examined alkaloid fate in H. axyridis larvae after consumption of two other ladybird species, one containing an alkaloid historically occurring within the predator's native range (isopropyleine) and one containing a novel alkaloid that does not (adaline). Our results indicate that H. axyridis rapidly chemically modifies the alkaloid to which it has been historically exposed to render it less harmful: this probably occurs outside of the gut. The novel, more toxic alkaloid persists in the body unchanged for longer. Our results suggest metabolic alkaloid specialisation, in spite of the diversity of chemically defended prey that the predator consumes. Physiological adaptations appear to have made H. axyridis a successful predator of other ladybirds; however, limitations are imposed by its physiology when it eats prey with novel alkaloids.

Invasions by ladybugs, ladybirds, and other predatory beetles

“…The extent of egg predation depends on the defensive alkaloids present in eggs of individual species (e.g., Agarwala and Dixon 1992;Sloggett and Davis 2010). A striking asymmetry occurs between H. axyridis and many ladybird species.…”

Detecting arthropod intraguild predation in the field

“…In general, DNA detection times are a few to many hours (McMillan et al, 2007;Greenstone et al, 2007), while detection using ELISA, can extend to days (Sopp and Sunderland, 1989;Symondson and Liddell, 1995). Results from GC-MS are highly variable, because target chemicals, especially defensive ones, can be broken down (Sloggett and Davis 2010;Sloggett et al 2011), sequestered or may remain in the predator as unmetabolised compounds. While Sloggett et al (2009) found that hippodamine from single H. convergens eggs persisted on average for 13.5 h in H. axyridis intraguild predators, Hautier et al (2008) found that adaline from a single A. bipunctata first instar larva could persist for many days.…”

Stage specific consumption and utilization of aphids, conspecific and heterospecific eggs by two species of Coccinella (Coleoptera: Coccinellidae)

“…Of the various stages, eggs are most likely to be attacked by predators, because they are immobile, poorly defended (Agarwala & Dixon, 1992;Felix & Soares, 2004;Michaud & Grant, 2004) and likely to be a high quality food (Gagné et al, 2002;Omkar et al, 2006). Many studies indicate that ladybird larvae fed conspecific (Gagné et al, 2002;Pervez et al, 2006;Roy et al, 2007) or heterospecific eggs (Pilipjuk et al, 1982;Pfannenstiel & Yeargan, 2002;Specty et al, 2003;De Clercq et al, 2005;Michaud & Jyoti, 2008) do better than when fed aphids whereas others indicate that conspecific and /or heterospecific eggs are inferior to aphids as food for ladybird larvae (Koide, 1962;Warren & Tadic, 1967;Takahashi, 1987;Rieder et al, 2008;Sloggett et al, 2009;Sloggett & Davis, 2010). Thus, the relative nutritive value of conspecific eggs, heterospecific eggs and aphids is a controversial issue.…”