Technical Comments

Comment on “Invasive Harlequin Ladybird Carries Biological Weapons Against Native Competitors”

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Science  20 Sep 2013:
Vol. 341, Issue 6152, pp. 1342
DOI: 10.1126/science.1241827

Abstract

Vilcinskas et al. (Reports, 17 May 2013, p. 862) proposed that infectious microsporidia of the invasive ladybird Harmonia axyridis act against intraguild predators, rather than ladybird alkaloid defenses. However, as both microsporidia and the harmonine defense alkaloid were administered to predators by microinjection rather than into the gut, such a conclusion is premature. Alkaloids also provide defense when predation occurs, whereas microsporidia act much later.

Vilcinskas et al. (1) proposed that the invasive harlequin ladybird beetle Harmonia axyridis defends itself against intraguild predation (IGP) by other ladybirds using parasitic microsporidia to which it is immune but other ladybirds are not. They dismiss earlier hypotheses based around the defensive chemistry of ladybirds (24) because microinjection of the H. axyridis alkaloid harmonine into larvae of another ladybird, Coccinella septempunctata, was not lethal. The authors suggest that this microbial defense could explain an IGP-related decline in native ladybirds.

Their study is open to several criticisms. First, the use of microinjection does not mimic the putative natural transfer of the microbe, especially through IGP. The situation is comparable to ladybird endosymbiotic male-killing bacteria. Although cross-genus microinjection of such endosymbionts reduces recipient fitness or survival (5), male killers are apparently rarely, if ever, transferred from ladybird to ladybird by predation, even by intraspecific egg cannibalism (6). Microbial defense by H. axyridis thus remains speculative until an interspecific transfer mechanism is demonstrated.

Chemistry remains a likely mode of H. axyridis defense against IGP. Vilcinskas et al. administered harmonine using microinjection. However, many defensive chemicals act in the gut or are enzymatically rendered toxic there [e.g., (79)]. Work on IGP and harmonine by Kajita et al. (3), discussed by Vilcinskas et al., used H. axyridis eggs frozen at –80°C: thus, the C. septempunctata mortality resulting from consuming these eggs was unlikely to have come from infection by living microbes. The possibility exists that apart from harmonine, H. axyridis might contain other untested alkaloids or defensive chemicals that protect it against natural enemies, including intraguild predators (4, 10).

The death of a C. septempunctata predator from microsporidian infection after several days confers very little benefit to the H. axyridis victim of the IGP. By contrast, the apparent toxicity of allospecific alkaloids can be near instantaneous and costly even when sublethal to ladybird intraguild predators (11). Furthermore, chemistry confers repellency as well as toxicity (4, 12). Kajita et al. found that H. axyridis eggs containing more harmonine were consumed less by C. septempunctata larvae (3). Repellency, possibly combined with fast-acting toxicity, would immediately protect potential ladybird victims of intraguild predation. For the alkaloid-bearing egg clutches, consumption of one egg would deter further egg consumption, and larvae and adults can protect themselves with alkaloid-laden defensive secretions.

Finally, if declines of native ladybirds have resulted from IGP at all, it is from H. axyridis IGP of other ladybirds, not through IGP of H. axyridis or its avoidance. The ladybird is a voracious intraguild predator and possesses at least some metabolic resistance to other ladybirds’ defensive alkaloids (1315).

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