Box 1.1. Collected to extinction?
The large blue butterfly (Maculinea arion) was reported to be in serious decline in southern England in the late 19th century, a phenomenon ascribed then to poor weather. By the mid-20th century this attractive species was restricted to some 30 colonies in south-western England. Only one or two colonies remained by 1974 and the estimated adult population had declined from about 100,000 in 1950 to 250 in some 20 years. Final extinction of the species in England in 1979 followed two successive hot, dry breeding seasons. Since the butterfly is beautiful and sought by collectors, excessive collecting was presumed to have caused at least the long-term decline that made the species vulnerable to deteriorating climate. This decline occurred even though a reserve was established in the 1930s to exclude both collectors and domestic livestock in an attempt to protect the butterfly and its habitat.
Evidently, habitat had changed through time, including a reduction of wild thyme (Thymus praecox), which provides the food for early instars of the large blue’s caterpillar. Shrubbier vegetation replaced short-turf grassland because of loss of grazing rabbits (through disease) and exclusion of grazing cattle and sheep from the reserved habitat. Thyme survived, however, but the butterflies continued to decline to extinction in Britain.
A more complex story has been revealed by research associated with reintroduction of the large blue to England from continental Europe. The larva of the large blue butterfly in England and on the European continent is an obligate predator in colonies of red ants belonging to species of Myrmica. Larval large blues must enter a Myrmica nest, in which they feed on larval ants. Similar predatory behavior, and/or tricking ants into feeding them as if they were the ants’ own brood, are features n the natural history of many Lycaenidae (blues and coppers) worldwide.
After hatching from an egg laid on the larval food plant, the large blue’s caterpillar feeds on thyme flowers until the molt into the final (fourth) larval instar, around August. At dusk, the caterpillar drops to the ground from the natal plant, where it waits inert until a Myrmica ant finds it. The worker ant attends the larva for an extended period, perhaps more than an hour, during which it feeds from a sugar gift secreted from the caterpillar’s dorsal nectary organ.
At some stage the caterpillar becomes turgid and adopts a posture that seems to convince the tend- ing ant that it is dealing with an escaped ant brood, and it is carried into the nest. Until this stage, immature growth has been modest, but in the ant nest the cater- pillar becomes predatory on ant brood and grows for 9 months until it pupates in early summer of the following year. The caterpillar requires an average 230 immature ants for successful pupation. The adult butterfly emerges from the pupal cuticle in summer and departs rapidly from the nest before the ants identify it as an intruder.
Adoption and incorporation into the ant colony turns out to be the critical stage in the life history. The complex system involves the “correct” ant, Myrmica sabuleti, being present, and this in turn depends on the appropriate microclimate associated with short-turf grassland. Longer grass causes cooler near-soil micro-climate favoring other Myrmica species, including M. scabrinodes that may displace M. sabuleti. Although caterpillars associate apparently indiscriminately with any Myrmica species, survivorship differs dramatically: with M. sabuleti approximately 15% survive, but an unsustainable reduction to < 2% survivorship occurs with M. scabrinodes. Successful maintenance of large blue populations requires that > 50% of the adoption by ants must be by M. sabuleti.
Other factors affecting survivorship include the requirements for the ant colony to have no alate (winged) queens and at least 400 well-fed workers to provide enough larvae for the caterpillar’s feeding needs, and to lie within 2 m of the host thyme plant. Such nests are associated with newly burnt grasslands, which are rapidly colonized by M. sabuleti. Nests should not be so old as to have developed more than the founding queen: the problem here being that the caterpillar becomes imbued with the chemical odors of queen larvae while feeding and, with numerous alate queens in the nest, can be mistaken for a queen and attacked and eaten by nurse ants.
Now that we understand the intricacies of the relationship, we can see that the well-meaning creation of reserves that lacked rabbits and excluded other grazers created vegetational and microhabitat changes that altered the dominance of ant species, to the detriment of the butterfly’s complex relationships. Over-collecting is not implicated, although climate change on a broader scale must play a role. Now five populations originating from Sweden have been reintroduced to habitat and conditions appropriate for M. sabuleti, thus leading to thriving populations of the large blue butterfly. Interestingly, other rare species of insects in the same habitat have responded positively to this informed management, suggesting an umbrella role for the butterfly species.