Evaluation of the palatability of chrysomelid larvae containing anthraquinones to birds

Abstract

Chrysomelid larvae of the subfamily Galerucinae, tribe Galerucini, are known to contain 1,8-dihydroxylated 9,10-anthraquinones. Since nonhydroxylated 9,10-anthraquinone is the active agent in several commercial products sold to protect seeds against birds, we suggested that the naturally occurring dihydroxylated anthraquinones of galerucine larvae may also act as protective devices against bird predation. Tits (Parus spp.) are potential predators of larvae of the tansy leaf beetle, Galeruca tanaceti, and the elm leaf beetle, Xanthogaleruca luteola. To investigate the palatability of these chrysomelid larvae to birds, we offered them with mealworms and Calliphora pupae, respectively, as controls in dual choice bioassays to eight singly kept, naive tits (five P. major and three P. ater individuals). The bioassays were limited to 5 days, during which larvae were offered daily for 2 h (X. luteola) and 3 h (G. tanaceti), respectively. Every day, the birds significantly avoided uptake of G. tanaceti and X. luteola. More than 98% of the control food was consumed daily, whereas the percentage of chrysomelid larvae totally eaten never surpassed 6.6% for G. tanaceti and 51.8% for X. luteola. In order to determine whether this avoidance was due to the anthraquinones of the chrysomelid larvae, mealworms and Calliphora pupae, respectively, were treated with these compounds in concentrations equivalent to the natural ones. Dual choice bioassays with treated and untreated prey were conducted, again for 5 days with a daily 2- or 3-h test period, respectively. The tits ate all or nearly all treated and untreated food items every day. However, during the 5-day test period the tits learnt to take up the control insects significantly earlier than the treated ones; the food containing anthraquinones was not consumed as readily as the control, which suggest aversive learning based on distastefulness. The efficiency of anthraquinones in protecting galerucine larvae against bird predation is discussed with special respect to learning behavior and factors which might delay or mask learning of avoidance.