Six-spot burnets: chemical weapons as nuptial gifts

Six-Spot Burnets, Zygaena filipendulae, are spectacular day flying moths. The contrast between their colour and the green meadows where they live makes them very obvious. Their body and forewing background are black, with a metallic green-blue sheen. Their forewings have six crimson-red spots. In addition they are large and heavy, and females like to perch conspicuously atop flower heads. You cannot miss a sitting burnet, but a flying one is even harder to miss: when they fly, a slow, buzzing, heavy flight, their crimson rear wings with a narrow black border become visible. As you could predict, this bright, black-with red spots contrasting colouration is a warning sign. Burnet moths are toxic, when they are injured, they release cyanide, a highly poisonous chemical. Cyanide compounds are found at some level in every life stage from egg to adult. The larvae sequester and store cyanogenic compounds from their food plants - Bird's Foot Trefoil, Lotus corniculatus - and all life stages are able to synthesize these chemicals themselves. However, production of the chemicals is costly, as larvae grow much more slowly when reared on varieties of Bird's Foot Trefoil lacking cyanogenic chemicals, as they have to synthesize them all themselves. There is a sudden loss of cyanogenic compounds from the last larval stage to the adult, and there also appears to be large variation in the amount of toxic chemicals in the adults. This could partly be explained by volatile hydrogen cyanide emissions by larvae - possibly as an antipredator strategy. Also, males convert some of their cyanogenic compounds into a pheromone; upon approaching a female, they release it. Females are able to determine how much pheromone a male is producing, the larger the quantity, the more likely the female is to accept him. But things get even more interesting. Mika Zagrobelny and co-workers, from the University of Copenhagen, collected Six-Spot Burnet larvae, pupa and adult from a local fallow field and made detailed measurements of the levels of cyanogenic compounds in the tissues of the different life stages, and also their toxic emissions. They found that females, as the larvae, emit hydrogen cyanide. Males are attracted to these chemical plumes, which form part of a pheromone cocktail produced by the female.

Average total cyanogenic compounds content in virgin and mated Z. filipendulae adults as well as in discarded males (which females would not mate with). Error bars are standard deviation. (figure modified from Zagrobelny et al. 2007).

The researchers then compared the cyanogenic compounds of virgin males and females, as well as mated males and females they paired up in the laboratory (see figure above). Virgin males and females had roughly similar levels of cyanogenic compounds. In contrast, after mating, females had larger levels, whereas males had lower levels. This indicates that during mating, males transfer some of these chemicals to the female, likely with the sperm. The levels of cyanogenic compounds in rejected males (males in an experimental pair that the females refused to mate with) were lower than average levels in virgin males, which suggests that females will mate preferentially with those males better loaded with chemical weapons. Why would the female benefit from acquiring more cyanide compounds. Possibly because the more she puts into eggs, the better defended they will be from predators, so this nuptial gift might be seen as a form of paternal behaviour. Alternatively, the female might gain through using this nuptial gift to produce more pheromone, attract further males and increase the vigour of her offspring.

A Six-Spot Burnet on Bird's Foot Trefoil

References
Zagrobelny M, Bak S, Olsen CE, & Møller BL (2007). Intimate roles for cyanogenic glucosides in the life cycle of Zygaena filipendulae (Lepidoptera, Zygaenidae). Insect biochemistry and molecular biology, 37 (11), 1189-97 PMID: 17916505