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Case Study: Critical parasitic relationship between ants and endangered butterflies

All five species of Maculinea butterfly in Europe are threatened by changing land use practices that convert meadows and pastures to scrub or developments. Maculinea arion, the Large Blue butterfly, became extinct in England in 1979 despite almost a century of efforts to preserve it. Early entomologists recognized the species' dependence on a specific larval food plant (Thymus) and the presence of Myrmica (red) ants. But even when preserves were set aside that included abundant Thymus and Myrmica, and the butterfly was protected from collectors, populations continued to decline.

Shortly before its extinction, a six year study was sponsored to determine the missing piece of the Maculinea arion puzzle and Jeremy Thomas and colleagues found it (reviewed in Elmes & Thomas 1992). Maculinea larvae dropped from their host plants after a certain age and were picked up by and brought to the nests of Myrmica ant species where they subsequently fed on ant larvae. Although all species of Myrmica will pick up Maculinea larvae indiscriminately - larvae produce sugar to attract ants and then use tactile signals and acquired scents to mimic ant larvae - larval survival is increased substantially in the nests of Myrmica sabuleti. Survival in an ants' nest depends on the nest being of sufficient size to support a hungry Maculinea to maturity and a larva being able to continually dupe the host ants into accepting it, which is easier with some ant species than others.

Several different species of Myrmica ants may co-occur in an area, each with its own critical micro-habitat. M. sabuleti prefer areas with short cropped grasses, and the warmer microclimate that results, more than other species. What butterfly preservation plans had not been taking into account was which Myrmica species was present on a preserve. Furthermore, in setting aside preserves, agricultural activities that favored M. sabuleti, such as mowing and grazing, were restricted leading to the gradual replacement of Maculinea's preferred host with ant species adapted to cooler micro-habitats.

Numerous studies have subsequently revealed similar species-specific dependencies for most Maculinea species on one or two related host plants and a different, single species of Myrmica. The relationship between the butterfly-ant species pairs has been a fertile area for comparative research on the evolution of parasitic adaptations which include the production of sugar and protein 'appeasements', larval stealth and armor, and tactile mimicry in predatory Maculinea species (such as M. arion), and the actual production of ant pheromones in 'cuckoo' species that are fed directly by the ants as one of their own larvae.

This research has also provided strategies for the preservation of Europe's Maculineas and the reintroduction of Maculinea arion to England from continental Europe. Managers now have specific information on 1) which host plant and ant species are necessary for the survival of various Maculinea species, 2) the microhabitat requirements of different Myrmica ant species, 3) the percentage of host plant and ant species overlap necessary in an area to support a Maculinea population (to ensure that sufficient larvae are found by the appropriate ant species), 4) the appropriate dispersion of host plants relative to ants nests (to ensure that too many larvae aren't brought to a single nest where they may compete and starve), and 5) the appropriate size and/or density of ant colonies (to support even a single Maculinea). Behavioral studies were crucial to a better understanding of the requirements of these butterflies.

Dingle, H., Carroll, S. P. and Loye, J. E. 1997. Conservation, behavior, and 99% of the world's biodiversity: Is our ignorance really bliss? In: Clemmons, J. R. and Buchholz, R. (eds.), Behavioral Approaches to Conservation in the Wild. Cambridge University Press, Cambridge. pp. 72-92.

Elmes, G.W. & Thomas, J. A. 1992. Complexity of species conservation in managed habitats: interaction between Maculinea butterflies and their ant hosts. Biodiversity and Conservation 1: 155-169.

Fiedler, K., Hoelldobler, B. and Seufert, P. 1996. Butterflies and ants: The communicative domain. Experientia 52: 14-24.

New, T. R., Pyle, R. M., Thomas, J. A., Thomas, C. D. and Hammond, P. C. 1995. Butterfly conservation management. Annu. Rev. Entomol. 40: 57-83.

Osborn, F. and Jaffe, K. 1997 Cooperation vs. exploitation: Interactions between Lycaenid (Lepidoptera: Lycaenidae) larvae and ants. J. Res. Lepid. 34: 69-82.

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