Leaf-scratching - a specialized behaviour of danaine butterflies (Lepidoptera) for gathering secondary plant substances.

Abstract

Danaine butterflies have long been recognized to be attracted to and "feed" at withered plants of certain genera (mainly of the Boraginaceae, Asteraceae, and Fabaceae) (for refs. see e.g. Pliske 1975, Boppr6 1978, 1981), which are characterized by the presence of pyrrolizidine alkaloids (PAs). The butterflies apply from their proboscides a fluid capable of dissolving PAs and then reimbibe it. The uptake of PAs does not provide energy the males require these secondary plant substances as precursors for the biosynthesis of a pheromone component (for review see Boppr6 1978). In addition, both sexes store them (Edgar et al. 1976, 1979, Boppr6 unpubl.), apparently for defense (see Rothschild et al. 1979, Eisner 1980, Conner et al. 1981, Boppr~ in prep.). Thus, the Danainae are typical pharmacophagous insects (cf. Boppr6 1983). Apart from danaines, other Lepidoptera (e.g. many Ithomiinae, Arctiidae, Ctenuchiidae; e.g. Pliske 1975, Boppr6 1981) and also Coleoptera (Gabonia (Chrysomelidae); Boppr6 and Scherer 1981) and Orthoptera (Zonocerus (Pyrgomorphidae); Boppr6 etal. 1983) have been found to gather PAs from dry plants, and some species of each of these orders are known to sequester PAs obtained with their larval food. These independent relationships between insects and PA-containing plants appear to represent a model system for comparative studies on co-evolution and adaptation (cf. Boppr6 and Schneider 1982). For danaines, not only withered plants but also nectar and damaged plants are sources of PAs, and they may even imbibe from carcasses of PA-storing insects (Owen 1971, Bernays et al. 1977, Boppr6 1981 and unpubl.). Danaine butterflies have also been reported scratching and sucking at living plants: Johnston and Johnston (1980 and pers. comm.) in Hong Kong observed species of Danaus and Euploea scratching leaves of Crotalaria retusa (Fabaceae) and imbibing the sap which oozed out. Similar behaviour has been noted in Australia by Sankowsky (in: Edgar and Culvenor 1975) at leaves of Parsonsia straminea (Apocynaceae), and on the Loyalty Islands, Edgar (pers. comm.) saw Danaus affinis scratching a leaf of Tournefortia argentia (Boraginaceae). Field observations from East Africa, reported here, provide some details on danaine butterflies' ability to damage fresh plant tissue in order to gain access to and obtain PAs. At the end of the rainy season in May 1982, in a valley near the Shimba Hills (Kwale District, Coast Province) in Kenya, large assemblages of Tirumala petiverana (Doubleday), together with several Danaus chrysippus (L.) and Amauris ochlea (Boisduval) were found on living plants of Heliotropium pectinatum Vaupel 1 (Boraginaceae) (Fig. 1). The butterflies, most if not all of which were males, congregated and imbibed sap from damaged parts of fresh leaves. This damage varied from a few surface scratches to whole sections of leaf torn away (Figs. 2-7). It was clearly seen (and documented on super-8 movie film) that this damage was caused by the butterflies themselves: from time to time they made scratching movements with a midleg (the fore-legs of Danainae are reduced as in all Nymphaloidea), which injured the leaf surface. Simultaneously, the butterflies sucked up oozing sap but sometimes they applied and reimbibed droplets with their proboscises as they do at dry plants. Almost all leaves of the Heliotropium population had holes of varying diameter (1-4 mm) made by flea beetles (Longitarsus gossypii Bryant, Chrysomelidae, Alticinae) (Figs. 5-7). Close inspection of leaves which were only slightly damaged by butterflies revealed that the danaines had scratched radially from these holes, and it appears that the edges of the holes release the chemical cues responsible for attraction of danaines, i.e. PAs or breakdown products of PAs, respectively. However, the butterflies usually did not scratch and suck individually but rather occurred in groups. Also, they attacked certain plants only. Very likely, scratching of a 'pioneer' butterfly at any beetle hole leads to an increase of PA-release, thus increasing the attractiveness of that particular leaf. Furthermore, it was apparent as at dry plants that conspecifics are an additional, visual attractant. In such ways, aggregations build up and the butterflies eventually scratch irregularly and affect neighbouring leaves. Such loci were found to be visited for several successive days, and within three weeks of observation, several plants were newly attacked. Numerous twigs with scratched and entirely wilted leaves were seen which were not attractive for butterflies; apparently these had previously served as PA-sources. Rhodogastria moths (Arctiidae) take advantage of danaine-damaged plants. Nocturnal observations revealed that the moths apparently preferred and assembled at those Heliotropium plants which had been recently scratched by danaines (Fig. 3). Rhodogastria were not seen to exhibit scratching behaviour themselves.