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Habitat quality and metapopulation effects are the main hypotheses that currently explain the disproportionate decline of insects in cultivated Holarctic landscapes. The former assumes a degradation in habitat quality for insects within surviving ecosystems, the latter that too few, small or isolated islands of ecosystem remain in landscapes for populations to persist. These hypotheses are often treated as alternatives, and this can lead to serious conflict in the interpretations of conservationists. We present the first empirical demonstration that habitat quality and site isolation are both important determinants of where populations persist in modern landscapes. We described the precise habitat requirements of Melitaea cinxia, Polyommatus bellargus and Thymelicus acteon, and quantified the variation in carrying capacity within each butterfly's niche. We then made detailed surveys to compare the distribution and density of every population of each species with the size, distance apart and quality of their specific habitats in all their potential habitat patches in three UK landscapes. In each case, within-site variation in habitat quality explained which patches supported a species' population two to three times better than site isolation. Site area and occupancy were not correlated in any species. Instead of representing alternative paradigms, habitat quality and spatial effects operate at different hierarchical levels within the same process: habitat quality is the missing third parameter in metapopulation dynamics, contributing more to species persistence, on the basis of these results, than site area or isolation. A reorientation in conservation priorities is recommended.

A polymorphism in growth rates was recently described affecting the larval development of the myrmecophilous butterfly Maculinea rebeli, spanning different years in a single insect population. The close integration of M. rebeli into the host ant colonies, facilitated by adaptations in behaviour and chemical mimicry, make extended larval development a successful strategy. Here we present additional data for M. rebeli and new data for Maculinea alcon (another cuckoo-feeding lycaenid) and the two myrmecophilous predators Maculinea arion and Microdon mutabilis (Diptera: Syrphidae). As predicted, M. alcon shows the same growth pattern as M. rebeli with a proportion of caterpillars developing in one year and the remainder over two years. This pattern holds in both northern and southern European populations, where M. alcon exploits different species of host. Against expectation, the same bimodal distribution of pre-pupation body weights, indicating one and two year developers, was found for the larvae of M. arion and M. mutabilis. As predators, both species are less closely integrated in their host ant colonies, suggesting that the polymorphism in growth rates is a more general adaptation to a myrmecophilous life style, arrived at by convergent evolution between the Maculinea and Microdon species. For predatory species we suggest that biennialism is an adaptation to the migratory behaviour of the host made possible by the predators' ability to fast over extended periods. We also hypothesize that M. arion represents an ancestral strategy in Maculinea butterflies and that the growth polymorphism might have become genetically fixed in the cuckoo-feeding species.

Although it has always been assumed that chemical mimicry and camouflage play a major role in the penetration of ant societies by social parasites, this paper provides the first direct evidence for such a mechanism between the larvae of the parasitic butterfly Maculinea rebeli and its ant host Myrmica schencki . In the wild, freshly moulted fourth–instar caterpillars, which have no previous contact with ants, appear to be recognized as ant larvae by foraging Myrmica workers, which return them to their nest brood chambers. Three hypotheses concerning the mechanism controlling this behaviour were tested: (i) the caterpillars produce surface chemicals that allow them to be treated as ant larvae; (ii) mimetic compounds would include hydrocarbons similar to those employed by Myrmica to recognize conspecifics and brood; and (iii) the caterpillar–s secretions would more closely mimic the profile of their main host in the wild, M. schencki , than that of other species of Myrmica . Results of behavioural bioassays and chemical analyses confirmed all three hypotheses, and explained the high degree of host specificity found in this type of highly specialized myrmecophile. Furthermore, although caterpillars biosynthesized many of the recognition pheromones of their host species (chemical mimicry), they later acquired additional hydrocarbons within the ant nest (chemical camouflage), making them near–perfect mimics of their individual host colony–s odour.

Caterpillars of Maculinea rebeli have two growth strategies for living underground as social parasites of Myrmica ant colonies. Laboratory experiments and field data show that 25% of caterpillars live ten months with ants before pupating, whereas 75% grow slowly, parasitizing their hosts for 22 months. Both types of caterpillar form apparently identical similar-sized pupae. This may be the first description in the animal kingdom of polymorphic growth rates spanning different years within the same population, yet without resulting (as in salmonid fish) in two morphologically distinct adult types with obvious differences in behaviour. We suggest that a balanced polymorphism has evolved in M. rebeli growth rates, representing the most efficient way of exploiting the limited, yet steady, daily supply of food available to cuckoo-feeding parasites of long-lived ant societies. Bet-hedging benefits would also accrue to adult butterflies producing a mixture of annual and biennial offspring. Despite ergonomic and other benefits, partial biennialism is unlikely to evolve unless slow-growing individuals have enhanced survival and can remain attached to their mobile hosts. We show that caterpillars become so closely protected by, and integrated with, their host colonies that slow growers experience no greater mortality over two years than fast growers over one, and are transported in preference to the ants' own larvae when the host colony moves nest site.

Metapopulation studies of single species have shown that the size and spatial arrangement of patches of assumed uniformly 'suitable' habitat can influence their population dynamics and persistence. We investigated whether variation in the spatial arrangement of 'suitable' habitat of varied quality within a single site can affect the abundance and persistence of interacting species. We accomplished this by extending a field-based spatial simulation model of four interacting species at two trophic levels (an endangered butterfly, its larval food-plant, and two ants). The habitat on sites with the same average and range of qualities was rearranged to give varying degrees of local spatial heterogeneity or 'site ruggedness'. We found that the ant species that acts as host to the butterfly caterpillars decreased with site ruggedness. The impact on the butterfly was more substantial: it often failed to persist on very rugged sites. Despite being free-ranging over the whole area, the butterfly's persistence depends on the arrangement of habitat quality at a finer spatial scale, due to its interactions with species possessing narrower habitat niches and more localized dispersal. Ruggedness also influenced the rate of recovery of the host ant, and hence community structure, for more than a century following the butterfly's extinction.