Lycaenid butterflies and ants

Introduction

Many Australian members of the butterfly family Lycaenidae (Blues, Coppers, Hairstreaks, Azures) have an unusual association with ants: they have specialized organs or glands that secrete substances that may attract, appease or reward ants. While not all lycaenid butterflies need ants, certain members of this family can only complete their life cycle in association with particular ant species. Each butterfly species is usually associated with a single ant species. The extent of the association varies.

Distribution

Members of the Family Lycaenidae are mainly found in the tropics. There are 125 species in Queensland, of which 102 are found north of Townsville. In contrast, only nine species are found in Tasmania. Many of the tropical and subtropical species are found in rainforest, but a few species occur in other habitats. A few are found in the arid and semi-arid environments of central Australia. Many species have limited distributions with specialised habitat preferences. Their populations tend to be localised, reflecting the patchy co-occurrence of the larval plant food and attendant ants. These factors make many lycaenids very vulnerable to habitat disturbance, and many species are threatened with extinction.

Other behaviours and adaptations

Ants are normally predators of butterfly larvae (caterpillars), however lycaenids have evolved a range of mechanisms to overcome predation. These mechanisms either deter the ants, or attract them by the secretion of compounds that are so attractive to ants that they will protect the larvae instead. Associations between the ants and the lycaenid larvae range from mutually beneficial relationships, where the ants get fed in return for feeding and/or protecting the larvae (for example, from parasitic wasps and predatory flies), to relationships where the larvae actually prey upon the ants.

Variations in the associations between ants and lycaenid larvae relate to the types of glands present and the chemicals produced by any one species of lycaenid. Three types of glands and the substances they produce are:

• small, single-celled glands scattered over the caterpillar's skin, present in all lycaenids, which produce substances that attract or appease ants. These are called pore cupola organs.
• a large gland located in the middle of the 7th abdominal segment, present in most lycaenids (except the subfamily Riodininae), which produces a thick liquid made up of sugars and amino acids. This is called the dorsal nectory organ or 'honey gland'.
• glands that are found on the 8th abdominal segment in most lycaenid subfamilies (but located on the metathorax (third segment of the thorax) in Riodininae). These are called dorsal eversible organs or 'tentacular organs': They take the form of long cylindrical tubes that can be everted (turned inside out), and are topped with a brightly coloured ring of spikes. When the tubes are retracted, a pale depression surrounded by hairs indicates their position. The function of these glands may be to attract or repel ants through the release of volatile chemicals, but this is not certain.

Ant attendance also varies with the larval (caterpillar) developmental stage (instar), with the later instars getting more attention than earlier ones. Other factors that may influence relationships are season, habitat and time of day.

Associations with ants include the following categories:

• Larvae that are not attended by ants, or only rarely associated with ants
• Larvae that are frequently attended by ants. These are called myrmecophilous ('ant-loving') associations. Within this category, there are two types of association:
• obligate myrmecophily: larvae that are always or regularly attended by a large number of ants
• facultative myrmecophily: larvae that are only sometimes attended, or only attended by a small number of ants.
• Larvae that either prey on ants or are fed by ants. These are called aphytophagous ('non-plant-eating') associations. In this category there are larvae that prey upon immature ants or larvae that feed on the regurgitations of ants. This category also includes species that prey upon, or feed on, secretions produced by bugs (Order Hemiptera).
• Larvae that are preyed upon by ants. This is a much smaller category. For example, the meat ant, Iridomyrmex purpureus, preys on the larvae of azure butterflies (Ogyris sp.) and a species of bull ant (Myrmecia sp.) preys on larvae of the Imperial Hairstreak (Jalmenus evagoras). Interestingly, both of these ant species actually attend other lycaenid larvae (Jalmenus ictinus and Theclinesthes, respectively).

These associations between lycaenids and ants usually benefit both partners (known as mutualism). However, even though the ants may benefit from harvesting food rewards offered to them by lycaenid larvae, they do not depend on lycaenids for survival and reproduction. Instead they forage on a wide range of other food resources. Similarly, most lycaenid larvae feed on the young leaves, flowers and seeds of plants, and are not completely dependant upon the ants they may be associated with. A small number of Australian lycaenids live as parasites within ant nests where they feed on the immature brood of their host ant.

Introduced pest ants are a direct threat to lycaenid butterflies because they compete with or destroy the indigenous ants upon which these butterflies depend.

Life history cycle

Lycaenid eggs are laid singly or in clusters on the underside of a leaf of the larval food plant. These eggs usually have a reticulated (net-like) pattern of ridges and intervening pits radiating out from a depression at the top, either obliquely, or at right angles. At the intersections of ridges, there are often knobs or spines.

In lycaenids there are usually five larval development stages (instars) before pupation. The final instar often spins a silk pad to which it attaches before becoming a pupa. Lycaenid larvae are relatively small compared with many caterpillars. They often hold their heads underneath their bodies, which are usually flattened and may be covered with small hairs.

The pupa is the non-feeding stage, in which the larval organs reorganize and transform into the adult organs. Lycaenid pupae sometimes have a dorsal honey gland in the middle of abdominal segment 7 and sound-producing structures between segments 5 and 6. In most species the undersides of the end segments of the abdomen are flattened and equipped with numerous minute anal hooks that fasten the pupa to a silk pad on a leaf. Other species lack these hooks and pupate directly in the soil.

The pupal cuticle splits to release the adult butterfly. Adults are generally small butterflies, and are known as Blues, Hairstreaks, Coppers or Azures, in reference to their blue or coppery wing colours.

References

• Braby, M. F. 2000. Butterflies of Australia. CSIRO Publishing, Melbourne.
• Eastwood, R. & Fraser, A. M. 1999. Associations between lycaenid butterflies and ants in Australia. Australian Journal of Ecology 24: 503-537.
• Kitching, R., Sheermeyer, E., Jones, R. and Pierce, N. E. (eds.). 1999. The Biology of Australian Butterflies (Monographs on Australian Lepidoptera Vol. 6); CSIRO Press, Sydney, 395 pp.
• Pierce, N. E., Braby, M. F., Heath, A., Lohman, D. J., Mathew, J., Rand, D. B., and Travassos, M. A.. 2002. The ecology and evolution of ant association in the Lycaenidae (Lepidoptera). Annual Review of Entomology 47: 733-771.